Association of Obesity With Hearing Impairment in Adolescents
Association of Obesity With Hearing Impairment in Adolescents
Association of Obesity With Hearing Impairment in Adolescents
com/scientificreports
Hearing loss (HL) is the third most common chronic physical condition in the United States. Obesity has
Received: 2 May 2018
become an increasingly important public health concern, as the prevalence in children, adolescents and
Accepted: 26 November 2018 adults has increased over the past few decades. The objectives of this study is to investigate whether
Published: xx xx xxxx obesity is associated with audiometric notches indicative of noise-induced hearing loss (NIHL), speech
frequency hearing loss (SFHL), and high frequency hearing loss (HFHL) in adolescent participants of the
National Health and Nutrition Examination Survey 2007–2010. The prevalence of overall audiometric
notches in the adolescent population was 16.0% with higher prevalence in females than males. The
prevalence of SFHL and HFHL were higher in males than females (SFHL, 7.3% vs. 5.4%, respectively;
and HFHL 14.3% vs. 8.1%, respectively). Obese adolescents had a higher adjusted OR to have
audiometric notches (OR = 1.93; 95% CI: 1.33–2.81) and HFHL (OR = 1.95; 95% CI: 1.19–3.21). Continued
preventative efforts towards reducing obesity might also help to reduce the risk for HL and NIHL.
Hearing loss (HL) is the third most common chronic physical condition in the United States1. The most common
preventable cause of HL is the damage to the auditory system caused by excessive noise exposure2,3. Although
the onset of this type of HL is usually slow, it progresses as long as the exposure continues. One of the first signs
of noise-induced hearing loss (NIHL) is an audiometric indication of a noise-induced hearing threshold shift
(NITS), usually defined as an “audiometric notch” at 3, 4, or 6 kHz. Henderson and colleagues4 reported increased
prevalence of audiometric notches in adolescents: 15.9% in NHANES 1998–1994 to 16.8% in NHANES 2005–
2006. Furthermore, damage to hearing at a young age can lead to exacerbated hearing loss later in life2. Data from
the National Health and Nutrition Examination Survey (NHANES) suggest that the prevalence of HL among
United States adolescents (12–19 years old) increased from 1994 to 2006 for both high frequency HL (HFHL)
and low frequency HL (LFHL). HFHL increased from 11.1% to 12.9% and LFHL increased from 5.2% to 6.5%4.
Obesity has become an increasingly important public health concern, as the prevalence in children, adoles-
cents and adults has increased over the past few decades both within the United States and worldwide. Among
U.S. adolescents aged 12 to 19 years, obesity prevalence increased between 1988–1994 and 2013–2014, from
10.5% (95%CI: 8.8, 12.5) to 20.6% (95%CI: 16.2, 25.6)5.
Health problems during childhood and adulthood associated with obesity include an increased risk of diabe-
tes, hypertension, nonalcoholic fatty liver disease, and depression6. Moreover, obesity has been associated with
unilateral low frequency HL, but not unilateral high frequency HL, in adolescent participants to NHANES 2005–
20067. There are no studies about potential risk factors for audiometric notches in adolescents. Therefore, the
objective of this study is to investigate whether obesity is associated with audiometric notches indicative of NIHL
and hearing loss in adolescents in a nationally representative survey.
Methods
Study population. NHANES is a cross-sectional, nationally representative survey of the non-institutional-
ized civilian population of the United States conducted by the National Center for Health Statistics at the Centers
for Disease Control and Prevention (CDC)8. Beginning in 1999, the survey has been conducted continuously and
released in 2-year cycles. For our study, we merged the publicly available files for NHANES cycles 2007–2008 and
2009–2010 using the NCHS recommendations8. The survey employed a multistage stratified probability sample
based on selected counties, blocks, households, and persons within households. During NHANES 2007–2010,
2,520 participants aged 12–19 years had complete audiometric data (response rate 97.8%, among 2577 partici-
pants who completed household interviews). We excluded participants with: 1) only a partial audio exam (miss-
ing information in any air conduction threshold, n = 147); 2) otoscopic screening exam of the ear canals and
1
Division for Toxicology and Human Health Services, Agency for Toxic Substances and Disease Registry, Atlanta, USA.
2
Office of Science, National Center for Environment Health, Centers for Disease Control and Prevention, Atlanta,
USA. 3Office of the Director, National Center for Environment Health, Centers for Disease Control and Prevention,
Atlanta, USA. Correspondence and requests for materials should be addressed to F.S. (email: [email protected])
n = 1469
Any Audiometric Notch, % (SE) 16.0 (0.95)
Bilateral Audiometric Notch, % (SE) 1.5 (0.39)
Unilateral Audiometric Notch, % (SE) 14.5 (1.02)
Speech Frequency Hearing Loss, % (SE) 6.3 (0.98)
High Frequency Hearing Loss, % (SE) 11.3 (1.51)
Male, % (SE) 51.8 (1.83)
Female, % (SE) 48.2 (1.83)
Age
12–15 years, % (SE) 51.1 (1.35)
18–19 years, % (SE) 48.9 (1.35)
Race/Ethnicity
Non-Hispanic White, % (SE) 63.9 (2.92)
Non-Hispanic Black, % (SE) 12.2 (1.10)
Mexican-American, % (SE) 11.8 (1.66)
Other (Other Hispanic and Other race), % (SE) 12.1 (1.77)
Poverty Income ratio
PIR ≤ 1, % (SE) 21.5 (1.62)
PIR > 1, % (SE) 78.5 (1.62)
Body Weight Status
Obese, % (SE) 18.4 (1.25)
Overweight, % (SE) 16.0 (1.06)
Underweight, % (SE) 3.3 (0.58)
Normal, % (SE) 62.3 (1.21)
Ever had 3 or more ear infections, % (SE) 36.0 (1.98)
Loud noise exposure for 5 or more hours per week, % (SE) 24.4 (1.44)
Smoking status
no smokers, % (SE) 27.2 (1.93)
second hand smokers exposure (SHS), % (SE) 56.8 (1.1.67)
smokers, % (SE) 16.0 (1.12)
Serum Cotinine ng/mL; GM (SE) 0.2 (0.02)
Hours of sedentary Activity; GM (SE) 6.2 (0.16)
Table 1. Weighted characteristics of adolescent participants (12–19 years of age) in NHANES 20072010.
eardrum for excessive or impacted ear cerumen (wax), physical abnormalities, or collapsing external ear canals
that was not normal (n = 475), or ear compliance ≤0.2 mL (N = 42), or pressure lower than −150 dekapascals
(daPa) (n = 18), and; 3) tinnitus based on the positive answer to the question “In the past 12 months, have you
been bothered by ringing, roaring or buzzing in your ears or head that lasted for five minutes or more?” (n = 119).
We, also, excluded participants that had missed information in the co-variates used in the analyses (n = 250).
Therefore, the total sample size used in our analyses was of 1469 adolescent participants.
Definition of Audiometric Notch and Hearing Loss. In this study, we define the presence of a
high-frequency audiometric notch as reported by Carroll et al.9 when:
• one or more of the thresholds (the softest sound a person can hear) at 3, 4, or 6 kHz exceeds the pure-tone
average (PTA) of the 0.5 and 1 kHz thresholds by 15 dB or more, and
• the 8 kHz threshold is at least 5 dB lower (better) than the maximum threshold in the 3, 4, or 6 kHz range.
Similar to other studies using NHANES, we used the average of four audiometric frequencies at 0.5, 1, 2, and
4 kHz to define the speech frequency (SF) PTA10,11 and the average of the three audiometric frequencies at 3, 4,
and 6 kHz to define an high frequency (HF) PTA4,10,11. We used a PTA of 15 dB HL or greater in either ear as a
Table 2. Estimated population prevalence % (95% CI) of audiometric notches and hearing Loss in US
adolescents aged 12 to 19 years, NHANES 2007–2010.
cutoff threshold for both the SF and HF PTA to define speech frequency hearing loss (SFHL) and high frequency
hearing loss (HFHL), respectively4,7,11.
Audiometric Notches
Model 1 Model 2
n. case/n. total 235/1469 233/1460
Male Referent Referent
Female 1.47 (1.06, 2.03) 1.51 (1.07, 2.11)
Age
12–15 years Referent Referent
16–19 years 0.91 (0.66, 1.27) 0.88 (0.63, 1.23)
Race/Ethnicity
Non-Hispanic White Referent Referent
Non-Hispanic Black 0.70 (0.51, 0.97) 0.69 (0.49, 0.96)
Mexican-American 1.22 (0.81, 1.84) 1.23 (0.83, 1.84)
Other (Other Hispanic and Other race) 0.95 (0.59, 1.51) 0.95 (0.60, 1.52)
Poverty Income ratio
PIR ≤ 1 1.01 (0.67, 1.51) 0.99 (0.66, 1.47)
PIR > 1 Referent Referent
Obese 1.93 (1.33, 2.81) 1.94 (1.34, 2.82)
Overweight 0.84 (0.52, 1.34) 0.83 (0.51, 1.35)
Underweight 1.12 (0.28, 4.52) 1.11 (0.27, 4.58)
Normal Referent Referent
No smokers Referent Referent
Second hand smokers exposure (SHS), 1.45 (1.04, 2.00) 1.44 (1.04, 2.00)
Smokers 1.26 (0.69, 2.31) 1.28 (0.69, 2.37)
Ever had 3 or more ear infections?
Yes 1.05 (0.75, 1.47) 1.06 (0.75, 1.49)
No Referent Referent
Loud noise exposure for 5 or more hours per week?
Yes 1.42 (0.76, 2.65) 1.43 (0.77, 2.68)
No Referent Referent
Hours sedentary activity(natural log-transformed) — 0.92 (0.74, 1.16)
Table 3. Multivariate logistic regression adjusted OR (95% CL) of having any audiometric notch for US
adolescents aged 12 to 19 years, NHANES 2007–2010 using.
playing cards, watching television, or using a computer. Excluding the time spent sleeping, how much time do
you usually spend sitting on a typical day?’ Since the variable was right skewed, it was naturally log-transformed.
Statistical Methods. All analyses were performed using the Mobile Exam Center weight as recommended
by NCHS, and to account for the complex sampling design and non-response of NHANES8. SAS 9.3 (SAS
Institute, Cary, NC) and SAS-Callable SUDAAN 10 (Research Triangle Institute, Research Triangle Park, NC)
was used for all statistical analyses. We used logistic regression to calculate adjusted odds ratios (ORs) and 95%
CIs for the audiometric notch and the hearing loss outcomes. Preliminary analyses did not found any significant
interaction term between the predictors (p > 0.10). Statistical tests for linear trends were conducted by modeling
ordinal variable using integer values. Two models, utilizing the various covariates were run: (1) model 1 included
age, sex, race/ethnicity, obesity, PIR, ear infections, loud noise exposure and smoking; (2) and, as sensitivity anal-
yses, model 2 included the covariates in model 1 plus hours of sedentary activity.
Results
Table 1 shows the characteristics of the population. Among adolescents, 63.9% were non-Hispanic white;
48.2% were female; 18.4% were obese, and 21.5% were from families with income at or below the poverty level.
Thirty-six percent and 24.4% of adolescents reported three or more ear infections or exposure to loud noise for 5
or more hours per week, respectively. Second hand smokers were 56.8% and 16.0% were smokers. The weighted
prevalence of audiometric notches, SFHL and HFHL in adolescents was 16.0%, 6.3%, and 11.3%, respectively.
Audiometric Notches. Table 2 shows the prevalence of overall audiometric notches. Females had a higher
prevalence of overall notches than males (18.2% vs 13.9%, χ2 p value = 0.06). The weighted prevalence of audio-
metric notches in obese adolescents was higher compared to normal weight adolescents (24.8% vs 14.7%).
In multivariate logistic regression analyses (Table 3), obese adolescents had higher odds to have audiometric
notches as normal weight adolescents [adjusted OR (aOR) = 1.93; 95% CI: 1.33–2.81. p trend = 0.002). Further
analyses with hours of sedentary activity (Table 3, Model 2), did not change the statistical significance asso-
ciation. As shown in Table 3, female adolescents had higher odds to have audiometric notches compared to
males (aOR = 1.47; 95% CI: 1.06–2.03) and those exposed to SHS had higher odds to have audiometric notches
Table 4. Adjusted OR (95% CL) from multivariate logistic regression of having hearing loss for US adolescents
aged 12 to 19 years, NHANES 2007–2010.
compared to those not exposed to tobacco (aOR = 1.45; 95% CI: 1.04–2.00). Further analyses with hours of sed-
entary activity (did not change the statistical significance association (Table 3, Model 2).
Speech Frequency Hearing Loss (SFHL). The prevalence of SFHL was 7.3% in males and 5.4% in females
(Table 2). The weighted prevalence of SFHL in obese adolescents was higher compared to normal weight adoles-
cents (8.5% vs 5.4%), but the difference was not statistically significant. In multivariate analysis no statistically
significant association was found between SFHL and body weight status (Table 4).
High Frequency Hearing Loss. The prevalence of HFHL (Table 2) was 14.3% among males and 8.1%
among female adolescents, and the difference was statistically significant (χ2 p value = 0.02). The weighted prev-
alence of HFHL in obese adolescents was statistically significant higher compared to normal weight adolescents
(17.9% vs 5.4%), (Table 2). In multivariate analyses (Table 4), obese adolescents had higher odds to have HFHL
compared to the normal weight adolescents (aOR = 1.95; 95% CI: 1.19–3.21. p trend < 0.05) (Table 4, Model 1).
The association remained when the hours of sedentary activity was, further, added as co-variate in the model
(Table 4, Model 2). Furthermore, the odds of having HFHL were higher in smokers (aOR = 3.07; 95% CI: 1.14–
8.21) compared to non-smokers (Table 4, Model 1).
Discussion
In the present study conducted using data from the NHANES 2007–2010 surveys we found that obesity was
associated with increase odd of having audiometric notches and high frequency hearing loss, but not with speech
frequency HL. These findings are notable because of the potential impact that hearing impairment at high fre-
quency can have on the social behavior of children and adolescents. Children with HL are more likely to expe-
rience academic difficulties, have behavioral problems, and demonstrate lower performance in oral language,
compared with their peers with normal hearing14. Although the primary objective in this study was the potential
association of obesity with hearing impairment, we found that tobacco exposure was, also, associated with audio-
metric notches and HFHL. In a previous analyses of adolescent participants of the NHANES 2005–2006, Lalwani
et al.7,15 found that obesity7 and serum cotinine15 were associated with low frequency HL, but not unilateral high
frequency HL. Although, there is a scarcity of epidemiological studies on the association of hearing impairment
with body weight status in adolescents, several studies have reported an association of obesity with hearing loss
in adults. In a longitudinal population-based cohort study (1993–95 to 2009–10), Cruickshanks et al.16 followed
up 1925 participants (mean age 60.7 years at baseline) with a normal hearing baseline. They found that smoking
and obesity were predicted risk factors for hearing loss (defined as a hearing threshold >25 dB of the pure tone
average of 0.5, 1, 2, and 4 kHz in either ear). In a cross-sectional study comprising 61,052 Korean adults 30 years
and older (20.13% female), Kim et al.17 reported that severely obese (BMI ≥ 30 kg/m2) persons had higher OR of
hearing loss. Obesity was slightly associated with HL. Üçler et al.18 reported an association between obesity and
hearing threshold in women aged 18–40 years. The associations were statistically significant at high frequencies
of 4, 6, and 8 kHz, but not at lower frequencies.
In a prospective study conducted among 68421 women participants in the Nurses’ Health Study II from 1989 to
2009, Curham et al.19 reported that higher BMI and larger waist circumference were associated with increased risk of
self-reported hearing loss. Conversely, Shargorodsky et al.20, in a study conducted in 26,917 adult men participants
in the Health Professionals Follow-up Study, did not find any association between obesity with increased risk of
self-reported hearing loss, but past smoking was independently associated with increased risk of hearing loss.
The biological plausibility of a role of obesity as risk factor for hearing impairment maybe through the per-
turbation of the adiponectin hormone. Hwang et al.21 hypothesized that plasma adiponectin mediates the effect
of obesity on hearing loss. Adiponectin is a protein hormone that modulates several metabolic processes, among
them glucose regulation and fatty acid oxidation22. Serum levels of adiponectin decrease with obesity23.
However, the best evidence supporting a role of obesity with the development of hearing impairment comes
from in vivo studies Tanigawa et al.24 found that compared to the wild-type (WT) mice, adiponectin-knockout
(APN-KO) mice had exacerbated hearing impairment, particularly in the high frequency range, with reduced
cochlear blood flow and capillary density of the stria vascularis. The hearing impairment was prevented
in APN-KO mice that were supplemented with adiponectin. Compared to the control group, Hwang et al.25
found that the auditory brainstem response threshold was significantly higher at high frequencies in mice with
diet-induced obesity (DIO). Although susceptibility to damage from noise exposure is highly variable in the
general population26, the potential reduction of cochlear blood flow in obese adolescents might make them more
susceptible to the harmful effects of noise.
Our study has several limitations. The cross-sectional nature of this study limits the inferences that can be
made based on the results. The associations reported in this study could be biased by uncontrolled factors such as
genetic predisposition, otosclerosis, hypertension, diabetes, ototoxic medication, and exposure to ototoxic sub-
stances27; however, we adjusted the models for several important confounding factors. A major study limitation is
the measurement of audiometric thresholds at a single point in time, since the identified audiometric notches may
only represent temporary threshold shifts. Concerns have been raised about potential false-positive rates of high
frequency audiogram notches, such as 6 and 8 kHz, which might be due to high subject variability and calibration
error for TDH-type headphones28.
Conclusion
Being obese was associated with NIHL and hearing loss. Health care professionals should be aware of the
increased risk of damage to hearing among their patients with obesity. Since hearing impairment often progresses
insidiously for years before being self-perceived or diagnosed29, early basic hearing screenings such as whisper
or finger rub tests may provide early diagnosis and opportunities for noise prevention counselling and access to
hearing aids30. Continued preventative efforts towards reducing obesity, should also have a positive impact among
adolescents at risk for NIHL and hearing loss.
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Acknowledgements
We would like to thank our colleagues at the CDC National Center for Health Statistics who conduct NHANES
surveys and our colleagues at the National Institute for Occupational Safety and Health who analyze the NHANES
audiograms. DISCLAIMER: The findings and conclusions in this report are those of the authors and do not
necessarily represent the official position of CDC/ATSDR.
Author Contributions
Conceived and designed the study: Franco Scinicariello, Yulia Carroll, John Eichwald. Performed the analysis:
Franco Scinicariello. Analyzed the data: Franco Scinicariello, Yulia Carroll, John Eichwald, John Decker, Patrick
N. Breysse. Prepared Tables 1–3: Franco Scinicariello, Yulia Carroll. Wrote the paper: Franco Scinicariello, Yulia
Carroll, John Eichwald, John Decker, Patrick N. Breysse.
Additional Information
Competing Interests: The authors declare no competing interests.
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