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Medical Science Monitor: International Medical Journal of Experimental and Clinical Research logoLink to Medical Science Monitor: International Medical Journal of Experimental and Clinical Research
. 2017 Jan 22;23:377–397. doi: 10.12659/MSM.899589

Sex-Related Cochlear Impairment in Cigarette Smokers

Grażyna Lisowska 1,A,B,C,E,F,G,, Jerzy Jochem 2,A,B,C,E,F,G, Agata Gierlotka 1,A,B,C,D,E,F,G, Maciej Misiołek 1,A,B,C,E,F,G, Wojciech Ścierski 1,A,B,C,D,E,F,G
PMCID: PMC5282963  PMID: 28110343

Abstract

Background

A number of studies have documented the influence of cigarette smoking on hearing. However, the association between sex and hearing impairment in smokers as measured by otoacoustic emissions (OAEs) has not been clearly established. The aim of this study was to analyze sex-specific effects of smoking on hearing via conventional and ultra-high-frequency pure tone audiometry (PTA), and OAEs, specifically spontaneous OAEs, click-evoked OAEs, and distortion-product OAEs.

Material/Methods

The study included 84 healthy volunteers aged 25–45 years (mean 34), among them 46 women (25 non-smokers and 21 smokers) and 38 men (16 non-smokers and 22 smokers). The protocol of the study included otoscopic examination, tympanometry, low-, moderate-, and ultra-high-frequency PTA, evaluation of spontaneous click-evoked (CEAOEs) and distortion-product otoacoustic emissions (DPOAEs), assessment of the DP-grams for 2f1-f2 (f1 from 977 to5 164 Hz), and input/output function at L2 primary tone level of 40–70 dB SPL.

Results

Smokers and non-smokers did not differ significantly in terms of their hearing thresholds assessed with tone audiometry. Male smokers presented with significantly lower levels of CEAOEs and DPOAEs than both male non-smokers and female smokers.

Conclusions

Smoking does not modulate a hearing threshold determined with PTA at low, moderate, and ultra-high frequencies, but causes a significant decrease in OAE levels. This effect was observed only in males, which implies that they are more susceptible to smoking-induced hearing impairment. Sex-specific differences in otoacoustic emissions level may reflect influences of genetic, hormonal, behavioral, and/or environmental factors.

MeSH Keywords: Hearing Loss; Otoacoustic Emissions, Spontaneous; Smoking

Background

Our knowledge regarding the harmful effects of tobacco smoke on hearing is still limited. Smoking was shown to result in vascular lesions and changes in some characteristics of the blood, leading to hypoxia-induced injury of various tissues, including the organ of hearing [13]. Researchers from the University of Washington in Seattle (United States) and University of Melbourne (Australia) analyzed the 1980–2012 data on the prevalence of cigarette smoking in 187 countries. They showed that the number of smokers older than 15 years of age increased from 721 million in 1980 to roughly one billion (967 million) in 2012. Also, the total number of smoked cigarettes increased, from 4.96 billion to 6.25 billion annually. Currently, the population of male and female smokers is estimated at 31% and 6.2% worldwide, respectively; 30 years earlier, these were 41% and 10%, respectively. According to the WHO data from 2011, the number of adult smokers in Poland is 28% lower than in 1995. Nevertheless, 27.2% of adults in Poland smoke and mean cigarette consumption is 15.4 per day. The percentages of male and female smokers in Poland are estimated at 33.6% and 20.5% of the adult population, respectively. The vast majority of Polish smokers are individuals between 45 and 59 years of age (36%), with 62.5% having primary or vocational education and 43% currently unemployed [4].

Exposure to harmful components of cigarette smoke leads to disorders of lipid metabolism and vascular endothelial dysfunction, which is reflected by enhanced atherosclerosis and increase in blood viscosity [1,2,5,6]. Carbon oxide present in tobacco smoke is a substrate for carboxyhemoglobin synthesis. Despite markedly higher affinity than hemoglobin, carboxyhemoglobin delivers significantly less oxygen to the tissues [710]. The vasoconstrictive effect of nicotine results in an impairment of tissue perfusion, which may be associated with cellular dysfunction in the case of chronic exposure to tobacco smoke [1,2,5,9]. According to one hypothesis, the harmful effects of tobacco smoke on hearing are associated with the toxic dysfunction of nicotinic acetylcholine receptors (nAChRs), a vital component of the hearing pathway [11,12]. Moreover, the toxic components of cigarette smoke were shown to impair the redox system, which was reflected by enhanced tissue hypoxia and injury, inter alia impairment of the active mechanisms of the outer hair cells (OHCs) of the cochlea [1315]. Measurement of OAEs is the only available non-invasive test for selective analysis of the OHC activity, enabling simple, objective, and highly sensitive functional examination of the hearing organ [16,17].

The aim of this study was to analyze the sex-specific effect of cigarette smoking on the results of subjective and objective examination of hearing, namely ultra-high frequency PTA, spontaneous otoacoustic emission (SOAE), and CEOAE and DPOAE levels.

Material and Methods

The study included 84 healthy volunteers aged between 25 and 45 years (mean 34 years), among them 41 non-smokers (mean age 33.3 years) and 43 smokers (mean age 34.7 years). The sample comprised 46 women (25 non-smokers and 21 smokers) and 38 men (16 non-smokers and 22 smokers). None of the participants had a history of audiological impairment. The group of smokers included the individuals who smoked at least 15 cigarettes per day for at least 7 years. The group of non-smokers included only the individuals who had never smoked. The exclusion criteria of the study were: abnormal result of otoscopic examination, history of ear problems, conductive hearing impairment, exposure to noise and ototoxic factors, disorders of cholesterol metabolism, arterial hypertension, chronic metabolic disorders (such as diabetes mellitus or kidney diseases), head injuries associated with the loss of consciousness, family history of genetic-related hearing impairment, disorders of the central nervous system, other acute or chronic systemic conditions, and abnormal body mass index (BMI). Moreover, none of the women participating in this study used hormonal preparations. All the participants were white. Mean body height of the study subjects was 172 cm (range 155–190 cm).

The protocol of the study was approved by the Local Bioethics Committee at the Medical University of Silesia (decision no. KNW/0022/KBI/28/09). All the experiments were conducted in accordance with the Declaration of Helsinki (revision 6, 2008) regarding the principles of human experimentation. Written informed consents were obtained from all the participants prior to any procedure included in the study protocol.

The protocol of the study included history-taking, otoscopic examination, tympanometry, PTA, and the evaluation of different types of OAEs.

PTA included air-conduction audiometry at 250–8 000 Hz, bone-conduction audiometry at 250–400 Hz, and ultra-high-frequency PTA at 8 000–20 000 Hz. PTA was performed in a sound-treated room, using an AC-40 Interacoustics Audiometer.

All otoacoustic emission tests (CEOAEs, DPOAEs, and SOAEs) were conducted with an Echoport ILO292 analyzer system, version 6.0 (Otodynamics). Otoacoustic emissions were performed separately for each ear. Prior to the test, the software automatically checked the resonance of the external ear canal and the probe sealing. CEOAEs were recorded in a nonlinear mode with 80-millisecond clicks presented at 85±3 dB pSPL and at a 50 per second rate. Recordings were time-windowed from 2.5 to 20 milliseconds. The responses to a total of 260 sets of clicks were averaged above the noise rejection level of 45 dB. The ILO292 system averages into 2 alternate buffers: A and B. The signal is estimated from the (A+B)/2 waveform, and the noise from the A–B difference waveform. The reproducibility is defined as the zero-lag correlation coefficient between the A and B buffers. CEOAEs were measured within the range of 1.0–5.0 kHz; the overall CEOAE response was analyzed.

DPOAEs were measured using a 2-channel probe using the same ILO292 analyzer system. For CEOAEs, a soft adapter was used to provide precise adaptation of the probe to the wall of the external ear canal. The otoacoustic emissions evoked by 2 tonal signals of different frequencies (f1 and f2) in a constant relation (f2/f1=1.22) were recorded. The levels of primary tones were different: L1=71 dB SPL and L2=60 dB SPL (according to Neely’s and Gorg’s formula: L1=44+0.45×L2); the tones were delivered at a constant frequency ratio f2/f1=1.22. The DP-grams for 2f1–f2 were collected for the f2 frequencies of 842 Hz to 7996 Hz with the resolution of 4 points per octave. Subsequently, DPOAEs were tested at the following intensities of primary stimuli, and the distortion 2f1–f2 was analyzed. DPOAEs were tested as a function of DP-gram and the input/output function at L2=40 dB SPL, 45 dB SPL, 50 dB SPL, 55 dB SPL, 60 dB SPL, 65 dB SPL, and 70 dB SPL. The input/output function was analyzed at 1000 Hz, 1500 Hz, 2000 Hz, 3000 Hz, 4000 Hz, 5000 Hz, and 6000 Hz.

The CEOAEs were considered present at Resp ≥3 dB SPL and Repro >75%, whereas DPOAEs whenever the signal-to-noise ratio (S/N) was higher than at 3 dB, irrespective of frequency. Similar criteria were implemented in the case of SOAEs.

Statistical analysis was carried out with a Statistica 8.0 PL package (StatSoft, United States). Normal distribution of the analyzed variables was verified with the Shapiro-Wilk test. The Student t-test and the Mann-Whitney U-test were used for the intergroup comparisons of normally and non-normally distributed/ranked variables, respectively (non-smokers vs. smokers, female non-smokers vs. male non-smokers, female non-smokers vs. female smokers, male non-smokers vs. male smokers, and female smokers vs. male smokers). The Bonferroni correction for the repeated measurements was applied.

We did not conduct an ANOVA (except from CEOAE – Repro, Resp, Noise) due to the characteristics of data distribution (lack of normality) and their specific character (the measurements were taken at 5-unit intervals, up to a maximum value). Parametric tests could be used solely for DPOAE-noise.

The results of PTA and ultra-high frequency PTA were recorded to the nearest 5th unit of the interval scale. Due to lack of normal distribution, the Mann-Whitney U-test was used with Bonferroni correction for repeated measurements.

Since the results for DPOAE were not distributed normally, the Mann-Whitney U-test was used with Bonferroni correction for repeated measurements. The only variable with normal distribution was DPOAE (Noise); therefore, the Student t-test was conducted with Bonferroni correction for repeated measurements.

In the case of CEOAE, Resp (dB), Repro (%), and Noise (dB) variables were distributed normally; therefore, the Student t-test was used to compare them. Stab (%) was the only variable without a normal distribution; therefore, the Mann-Whitney U-test was conducted. No Bonferroni correction was used owing to lack of repeated measurements.

The statistical characteristics of the analyzed variables are presented as means and their standard deviations (SD). The threshold of statistical significance for all the tests was set at p<0.05.

Results

Hearing threshold assessed with PTA

Smokers and non-smokers did not differ significantly in terms of their hearing thresholds at 250–20 000 Hz. Nevertheless, the smokers presented with slightly higher hearing thresholds at all the frequencies examined (p>0.05): PTA thresholds at 250–8 000 (Figures 15) and PTA thresholds at ultra-high frequencies (Figures 610).

Figure 1.

Figure 1

PTA thresholds at 250–8 000 Hz in smokers (squares) and non-smokers (circles).

Figure 2.

Figure 2

PTA thresholds at 250–8 000 in male smokers (squares) and male non-smokers (circles).

Figure 3.

Figure 3

PTA thresholds at 250–8 000 in female smokers (squares) and female non-smokers (circles).

Figure 4.

Figure 4

PTA thresholds at 250–8 000 in male smokers (squares) and female smokers (circles).

Figure 5.

Figure 5

PTA thresholds at 250–8 000 in male non-smokers (squares) and female non-smokers (circles).

Figure 6.

Figure 6

PTA thresholds at high frequencies in smokers (squares) and non-smokers (circles).

Figure 7.

Figure 7

PTA thresholds at high frequencies in male smokers (squares) and male non-smokers (circles).

Figure 8.

Figure 8

PTA thresholds at high frequencies in female smokers (squares) and female non-smokers (circles).

Figure 9.

Figure 9

PTA thresholds at high frequencies in male smokers (squares) and female smokers (circles).

Figure 10.

Figure 10

PTA thresholds at high frequencies in male non-smokers (squares) and female non-smokers (circles).

Click-evoked otoacoustic emissions

The levels of CEOAEs is smokers were always lower than in non-smokers, but most of these differences did not prove significant on statistical analysis. The only statistically significant differences in the overall CEOAE levels were found when the results of male smokers were compared with those of male non-smokers (p=0.026) and female smokers (p=0.001) (Tables 15). This suggests that, in contrast to smoking women, male smokers are at increased risk of functional OHC impairment.

Table 1.

CEOAE levels in smokers and non-smokers.

Parameter Smokers Non-smokers p
n (ears) Mean SD n (ears) Mean SD
Resp dB 81 10.74 4.46 75 10.88 3.63 0.833
Repro % 81 92.59 6.11 75 92.56 6.76 0.975
Noise dB 81 −1.80 3.08 75 −1.65 3.51 0.791
Stab % 81 99.74 0.95 75 99.57 2.69 0.871

Table 2.

CEOAE levels in male smokers and female smokers.

Parameter Male smokers Female smokers p
n (ears) Mean SD n (ears) Mean SD
Resp dB 39 9.13 3.55 42 12.24 4.73 0.001
Repro % 39 90.74 6.82 42 94.31 4.84 0.009
Noise dB 39 −1.80 2.92 42 −1.79 3.25 0.983
Stab % 39 99.85 0.37 42 99.64 1.27 0.760

Table 3.

CEOAE levels in male non-smokers and female non-smokers.

Parameter Male non-smokers Female non-smokers p
n (ears) Mean SD n (ears) Mean SD
Resp dB 29 11.21 3.86 46 10.67 3.51 0.541
Repro % 29 93.90 5.96 46 91.72 7.16 0.159
Noise dB 29 −2.17 3.71 46 −1.33 3.39 0.329
Stab % 29 99.76 0.44 46 99.46 3.43 0.378

Table 4.

CEOAE levels in male smokers and male non-smokers.

Parameter Male smokers Male non-smokers p
n (ears) Mean SD n (ears) Mean SD
Resp dB 39 9.13 3.55 29 11.21 3.86 0.026
Repro % 39 90.74 6.82 29 93.90 5.96 0.047
Noise dB 39 −1.80 2.92 29 −2.17 3.71 0.662
Stab % 39 99.85 0.37 29 99.76 0.44 0.372

Table 5.

CEOAE levels in female smokers and female non-smokers.

Parameter Female smokers Female non-smokers p
n (ears) Mean SD n (ears) Mean SD
Resp dB 42 12.24 4.73 46 10.67 3.51 0.083
Repro % 42 94.31 4.84 46 91.72 7.16 0.048
Noise dB 42 −1.79 3.25 46 −1.33 3.39 0.520
Stab % 42 99.64 1.27 46 99.46 3.43 0.351

Distortion-product otoacoustic emissions (DP-gram function)

The analyzed groups did not differ significantly in terms of their DPOAE levels at various frequencies, both in SNR analysis and when the overall response level was considered. The only exception pertained to the level of DPOAEs at f2=1 685 Hz, which was significantly lower in male smokers than in male non-smokers. All the results are presented in Tables 610. Irrespective of the testing conditions, no significant intergroup differences were found with regards to the background noise level.

Table 6.

DPOAE levels in smokers and non-smokers.

Frequency Smokers Non-smokers p DP p noise p SNR
DP Noise SNR DP Noise SNR
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
842 Hz 4.19 5.91 −3.81 3.83 7.98 5.94 3.86 6.10 −4.41 3.86 8.27 5.49 1.000 0.996 1.000
1001 Hz 4.18 6.93 −5.84 3.53 10.02 5.87 5.36 7.56 −6.05 3.28 11.41 7.60 0.991 1.000 0.943
1184 Hz 6.77 7.67 −6.11 3.61 12.88 6.97 6.91 6.05 −7.02 3.36 13.92 5.85 1.000 0.737 0.992
1416 Hz 7.76 8.70 −6.58 3.80 14.34 7.73 8.59 8.09 −7.58 3.45 16.06 7.81 1.000 0.670 0.900
1685 Hz 8.28 6.91 −8.12 2.76 16.43 6.46 9.47 6.04 −7.67 2.76 17.14 6.82 0.972 0.990 1.000
2002 Hz 7.26 6.15 −9.12 2.60 16.38 5.77 7.75 7.23 −9.37 2.26 17.12 7.40 1.000 1.000 1.000
2380 Hz 6.10 7.15 −9.53 2.30 15.62 7.05 7.18 6.23 −9.98 2.52 17.16 6.20 0.990 0.967 0.855
2832 Hz 4.83 8.96 −10.31 2.34 15.15 8.15 7.45 6.96 −10.24 1.86 17.69 7.14 0.382 1.000 0.363
3369 Hz 7.31 6.78 −9.78 3.20 17.34 6.45 7.64 6.99 −10.08 1.85 17.72 7.26 1.000 1.000 1.000
4004 Hz 9.11 8.26 −9.77 2.02 19.00 7.92 10.30 6.42 −9.87 1.76 20.09 6.66 0.991 1.000 0.995
4761 Hz 10.11 8.62 −9.50 2.13 19.77 7.91 11.39 7.09 −9.43 2.21 20.83 6.78 0.989 1.000 0.997
5652 Hz 6.87 9.96 −9.25 2.38 16.11 9.17 7.27 8.66 −10.12 2.78 17.26 8.09 1.000 0.334 0.999
6726 Hz −0.62 10.57 −10.65 3.37 10.26 9.68 0.75 10.58 −11.39 2.60 12.14 9.95 0.999 0.811 0.967
7996 Hz −15.35 13.27 −13.13 2.13 −1.68 12.55 −12.17 13.10 −13.92 2.48 1.35 11.53 0.873 0.437 0.839

Table 7.

DPOAE levels in male smokers and female smokers.

Frequency Male smokers Female smokers p DP p noise p SNR
DP Noise SNR DP Noise SNR
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
842 Hz 2.93 6.21 −3.62 4.21 6.51 6.47 5.50 5.37 −4.00 3.44 9.50 4.99 0.546 1.000 0.309
1001 Hz 2.89 6.02 −5.76 3.02 8.65 5.40 5.59 7.64 −5.93 4.07 11.52 6.06 0.652 1.000 0.278
1184 Hz 5.51 7.71 −6.12 3.10 11.63 7.13 8.07 7.50 −6.09 4.10 14.16 6.64 0.834 1.000 0.740
1416 Hz 5.82 9.81 −6.86 3.68 12.69 8.14 9.75 6.97 −6.30 3.94 16.05 6.98 0.422 1.000 0.483
1685 Hz 6.73 6.57 −8.30 2.74 15.10 5.93 9.86 6.96 −7.94 2.79 17.80 6.77 0.379 1.000 0.515
2002 Hz 6.14 5.56 −9.06 2.49 15.20 5.46 8.40 6.58 −9.19 2.74 17.59 5.90 0.710 1.000 0.529
2380 Hz 4.68 7.01 −9.63 1.96 14.31 6.82 7.55 7.07 −9.42 2.62 16.97 7.11 0.578 1.000 0.672
2832 Hz 4.05 9.39 −10.22 2.58 14.28 8.48 5.64 8.54 −10.41 2.10 16.07 7.78 0.999 1.000 0.992
3369 Hz 6.53 6.82 −9.48 3.78 16.50 6.90 8.10 6.74 −10.09 2.50 18.19 5.92 0.987 0.998 0.966
4004 Hz 7.84 9.45 −9.56 1.73 17.63 9.13 10.41 6.71 −9.98 2.27 20.39 6.25 0.882 0.996 0.774
4761 Hz 8.55 9.49 −9.72 2.31 18.27 9.01 11.75 7.36 −9.28 1.91 21.34 6.30 0.682 0.996 0.610
5652 Hz 5.98 9.67 −8.77 2.01 14.75 9.21 7.80 10.29 −9.74 2.65 17.54 9.01 0.999 0.566 0.902
6726 Hz −0.96 9.67 −9.98 3.89 9.48 8.97 −0.26 11.57 −11.36 2.55 11.11 10.44 1.000 0.556 1.000
7996 Hz −15.24 13.81 −13.12 2.23 −2.11 12.78 −15.46 12.90 −13.14 2.07 −1.26 12.48 1.000 1.000 1.000

Table 8.

DPOAE levels in male non-smokers and female non-smokers.

Frequency Male non-smokers Female non-smokers p DP p noise p SNR
DP Noise SNR DP Noise SNR
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
842 Hz 5.47 6.35 −3.71 4.14 9.18 6.29 2.71 5.71 −4.90 3.61 7.61 4.82 0.572 0.954 0.979
1001 Hz 6.37 9.49 −5.24 3.81 11.61 9.71 4.75 6.14 −6.54 2.84 11.29 6.09 0.999 0.807 1.000
1184 Hz 7.16 6.40 −7.08 3.99 14.24 6.46 6.75 5.88 −6.98 2.92 13.71 5.48 1.000 1.000 1.000
1416 Hz 9.23 7.53 −7.11 3.45 16.05 8.35 8.19 8.48 −7.88 3.45 16.08 7.54 1.000 0.995 1.000
1685 Hz 11.42 5.02 −8.00 3.06 19.42 5.91 8.30 6.34 −7.47 2.58 15.77 7.01 0.204 0.999 0.179
2002 Hz 9.06 8.03 −8.80 2.09 17.86 8.80 6.95 6.64 −9.72 2.30 16.67 6.44 0.964 0.602 1.000
2380 Hz 7.09 7.27 −9.97 2.50 17.06 7.49 7.23 5.57 −9.98 2.55 17.22 5.34 1.000 1.000 1.000
2832 Hz 6.88 9.86 −10.75 1.68 17.64 10.17 7.80 4.30 −9.92 1.91 17.72 4.40 1.000 0.443 1.000
3369 Hz 7.22 8.76 −10.00 1.82 17.22 8.95 7.91 5.67 −10.14 1.89 18.05 6.01 1.000 1.000 1.000
4004 Hz 9.74 7.93 −9.78 1.77 19.32 8.19 10.64 5.33 −9.93 1.77 20.57 5.55 1.000 1.000 1.000
4761 Hz 10.91 6.83 −9.27 2.14 20.18 6.58 11.69 7.30 −9.53 2.27 21.23 6.94 1.000 1.000 1.000
5652 Hz 6.76 9.10 −10.14 2.68 16.90 8.43 7.59 8.45 −10.11 2.86 17.48 7.95 1.000 1.000 1.000
6726 Hz −0.90 12.07 −11.48 2.95 10.58 10.74 1.92 9.35 −11.33 2.36 13.24 9.31 0.985 1.000 0.981
7996 Hz −11.06 12.84 −14.39 2.57 3.33 11.75 −12.79 13.35 −13.65 2.42 0.22 11.38 1.000 0.971 0.986

Table 9.

DPOAE levels in male smokers and male non-smokers.

Frequency Male smokers Male non-smokers p DP p noise p SNR
DP Noise SNR DP Noise SNR
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
842 Hz 2.93 6.21 −3.62 4.21 6.51 6.47 5.47 6.35 −3.71 4.14 9.18 6.29 0.758 1.000 0.711
1001 Hz 2.89 6.02 −5.76 3.02 8.65 5.40 6.37 9.49 −5.24 3.81 11.61 9.71 0.690 1.000 0.864
1184 Hz 5.51 7.71 −6.12 3.10 11.63 7.13 7.16 6.40 −7.08 3.99 14.24 6.46 0.994 0.984 0.774
1416 Hz 5.82 9.81 −6.86 3.68 12.69 8.14 9.23 7.53 −7.11 3.45 16.05 8.35 0.748 1.000 0.716
1685 Hz 6.73 6.57 −8.30 2.74 15.10 5.93 11.42 5.02 −8.00 3.06 19.42 5.91 0.012 1.000 0.040
2002 Hz 6.14 5.56 −9.06 2.49 15.20 5.46 9.06 8.03 −8.80 2.09 17.86 8.80 0.694 1.000 0.867
2380 Hz 4.68 7.01 −9.63 1.96 14.31 6.82 7.09 7.27 −9.97 2.50 17.06 7.49 0.892 1.000 0.781
2832 Hz 4.05 9.39 −10.22 2.58 14.28 8.48 6.88 9.86 −10.75 1.68 17.64 10.17 0.958 0.985 0.853
3369 Hz 6.53 6.82 −9.48 3.78 16.50 6.90 7.22 8.76 −10.00 1.82 17.22 8.95 1.000 0.999 1.000
4004 Hz 7.84 9.45 −9.56 1.73 17.63 9.13 9.74 7.93 −9.78 1.77 19.32 8.19 0.997 1.000 0.999
4761 Hz 8.55 9.49 −9.72 2.31 18.27 9.01 10.91 6.83 −9.27 2.14 20.18 6.58 0.957 0.999 0.989
5652 Hz 5.98 9.67 −8.77 2.01 14.75 9.21 6.76 9.10 −10.14 2.68 16.90 8.43 1.000 0.227 0.991
6726 Hz −0.96 9.67 −9.98 3.89 9.48 8.97 −0.90 12.07 −11.48 2.95 10.58 10.74 1.000 0.571 1.000
7996 Hz −15.24 13.81 −13.12 2.23 −2.11 12.78 −11.06 12.84 −14.39 2.57 3.33 11.75 0.962 0.474 0.693

Table 10.

DPOAE levels in female smokers and female non-smokers.

Frequency Female smokers Female non-smokers p DP p noise p SNR
DP Noise SNR DP Noise SNR
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
842 Hz 5.50 5.37 −4.00 3.44 9.50 4.99 2.71 5.71 −4.90 3.61 7.61 4.82 0.311 0.980 0.717
1001 Hz 5.59 7.64 −5.93 4.07 11.52 6.06 4.75 6.14 −6.54 2.84 11.29 6.09 1.000 0.999 1.000
1184 Hz 8.07 7.50 −6.09 4.10 14.16 6.64 6.75 5.88 −6.98 2.92 13.71 5.48 0.997 0.976 1.000
1416 Hz 9.75 6.97 −6.30 3.94 16.05 6.98 8.19 8.48 −7.88 3.45 16.08 7.54 0.996 0.482 1.000
1685 Hz 9.86 6.96 −7.94 2.79 17.80 6.77 8.30 6.34 −7.47 2.58 15.77 7.01 0.982 0.999 0.901
2002 Hz 8.40 6.58 −9.19 2.74 17.59 5.90 6.95 6.64 −9.72 2.30 16.67 6.44 0.989 0.993 1.000
2380 Hz 7.55 7.07 −9.42 2.62 16.97 7.11 7.23 5.57 −9.98 2.55 17.22 5.34 1.000 0.991 1.000
2832 Hz 5.64 8.54 −10.41 2.10 16.07 7.78 7.80 4.30 −9.92 1.91 17.72 4.40 0.863 0.976 0.965
3369 Hz 8.10 6.74 −10.09 2.50 18.19 5.92 7.91 5.67 −10.14 1.89 18.05 6.01 1.000 1.000 1.000
4004 Hz 10.41 6.71 −9.98 2.27 20.39 6.25 10.64 5.33 −9.93 1.77 20.57 5.55 1.000 1.000 1.000
4761 Hz 11.75 7.36 −9.28 1.91 21.34 6.30 11.69 7.30 −9.53 2.27 21.23 6.94 1.000 1.000 1.000
5652 Hz 7.80 10.29 −9.74 2.65 17.54 9.01 7.59 8.45 −10.11 2.86 17.48 7.95 1.000 1.000 1.000
6726 Hz −0.26 11.57 −11.36 2.55 11.11 10.44 1.92 9.35 −11.33 2.36 13.24 9.31 0.996 1.000 0.994
7996 Hz −15.46 12.90 −13.14 2.07 −1.26 12.48 −12.79 13.35 −13.65 2.42 0.22 11.38 0.997 0.991 1.000

Active and passive mechanisms of the cochlea (I/O function of DPOAEs)

Aside from significant differences between smokers and non-smokers overall, we also found significant differences between male smokers and male non-smokers, as well as between male and female smokers. This suggests that smoking may impair the cochlear mechanisms, but predominantly in males. Irrespective of the testing conditions, no significant intergroup differences were found with regards to the background noise level.

Smokers presented with significantly lower levels of DPOAEs than non-smokers at the following frequencies (f2) and stimulus intensities (L2): 1000 Hz +60 dB SPL and 45 dB SPL, 1 500 Hz +70 dB SPL, 65 dB SPL, 60 dB SPL and 40 dB SPL, 2 000 Hz +60 dB SPL or 55 dB SPL, and 3000 Hz +60 dB SPL, 50 dB SPL and 45 dB SPL. These findings suggest that smoking impairs both active and passive mechanisms of the cochlea, especially at lower and moderate frequencies (1–3 kHz).

Compared to male non-smokers, male smokers presented with significantly lower DPOAE levels in an I/O function at the following frequencies (f2) and stimulus intensities (L2): 1 000 Hz +60 dB SPL, 50 dB SPL, 45 dB SPL and 40 dB SPL, 1500 Hz +70 dB SPL and 65 dB SPL, 2 000 Hz +70 dB SPL, 65 dB SPL, 60 dB SPL and 55 dB SPL, 3000 Hz +45 dB SPL and 40 dB SPL, and 4000 Hz +70 dB SPL. Unlike in men, female smokers and non-smokers did not differ significantly in terms of their DPOAE levels in an I/O function.

Comparative analysis of male and female smokers showed that the former presented with significantly lower DPOAE levels in an I/O function at the following frequencies (f2) and stimulus intensities (L2): 1000 Hz +60 dB SPL, 55 dB SPL, 50 dB SPL and 45 dB SPL, 2000 Hz +70 dB SPL, 65 dB SPL, 60 dB SPL and 40 dB SPL, and 5000 Hz + 70 dB SPL, 60 dB SPL and 55 dB SPL. In contrast, male and female non-smokers did not differ significantly in terms of their DPOAE levels in an I/O function. All the results are presented in Tables 1115.

Table 11.

DPOAE levels – I/O analysis in smokers and non-smokers.

L2 level dB SPL Smokers Non smokers p Smokers Non-smokers p
n mean SD n mean SD n mean SD n mean SD
1000 Hz DPOAE levels 1000 Hz SNR analysis
70 82 9.38 5.95 80 9.67 6.69 0.766 82 12.19 5.56 80 13.06 6.64 0.368
65 84 6.88 6.96 81 7.31 5.86 0.666 84 9.61 6.01 81 10.86 6.23 0.192
60 84 6.14 7.34 78 7.16 5.33 0.319 84 8.81 6.82 78 11.03 5.77 0.027
55 82 5.08 6.32 77 5.43 7.12 0.745 82 9.15 5.75 77 9.82 6.31 0.482
50 79 3.27 6.61 75 3.76 7.58 0.675 79 8.00 6.25 75 9.18 7.16 0.276
45 75 0.96 7.04 72 2.79 6.11 0.095 75 6.09 6.40 72 8.44 5.83 0.022
40 64 −2.44 9.69 68 −0.73 8.43 0.282 64 3.34 8.17 68 5.55 7.54 0.108
1500 Hz DPOAE levels 1500 Hz SNR analysis
70 85 11.92 7.65 81 13.49 5.45 0.131 85 16.80 7.85 81 20.38 6.41 0.002
65 84 10.70 8.33 80 12.41 5.30 0.122 84 15.39 8.00 80 18.17 5.95 0.013
60 85 9.56 7.09 79 10.97 5.88 0.169 85 14.76 6.19 79 16.75 5.99 0.039
55 84 7.55 8.04 80 8.53 8.26 0.441 84 13.26 7.18 80 14.63 7.76 0.242
50 83 5.22 8.62 80 6.47 7.52 0.324 83 11.40 7.05 80 12.92 6.86 0.167
45 79 3.38 7.79 79 4.95 7.28 0.192 79 10.34 5.99 79 12.07 6.84 0.094
40 76 0.02 9.63 78 1.82 8.62 0.223 76 7.04 7.82 78 9.83 7.81 0.028
2000 Hz DPOAE levels 2000 Hz SNR analysis
70 86 11.90 5.31 81 12.07 5.78 0.841 86 19.75 6.33 81 21.27 6.28 0.122
65 86 10.89 5.51 81 11.24 5.81 0.690 86 18.00 6.06 81 19.65 6.13 0.082
60 86 8.67 7.43 80 10.16 6.17 0.163 86 16.23 7.35 80 18.60 6.81 0.033
55 84 7.62 5.92 81 8.23 6.35 0.523 84 15.34 6.07 81 17.41 6.45 0.035
50 84 4.93 7.56 79 6.03 7.65 0.358 84 13.55 7.18 79 15.03 7.57 0.202
45 83 2.90 6.44 80 2.88 8.68 0.984 83 11.77 6.17 80 12.63 7.76 0.431
40 76 0.05 7.73 79 −1.13 10.40 0.426 76 8.88 6.36 79 8.86 9.63 0.991
3000 Hz DPOAE levels 3000 Hz SNR analysis
70 85 10.19 5.57 81 11.08 5.67 0.310 85 20.45 5.85 81 22.11 6.07 0.073
65 85 9.18 6.23 81 9.93 6.50 0.446 85 18.54 6.13 81 19.81 6.93 0.210
60 86 7.42 6.41 81 8.69 5.84 0.184 86 16.59 6.54 81 18.60 5.83 0.038
55 86 5.98 7.22 82 7.20 7.27 0.277 86 15.56 6.73 82 17.20 7.30 0.130
50 86 3.94 8.12 82 5.65 6.34 0.131 86 13.89 6.77 82 15.84 5.93 0.049
45 83 0.29 11.46 82 2.79 7.70 0.102 83 10.43 9.64 82 13.76 7.59 0.015
40 79 −0.98 10.26 80 0.65 7.27 0.248 79 10.07 8.55 80 11.66 6.73 0.196
4000 Hz DPOAE levels 4000 Hz SNR analysis
70 86 13.74 6.29 80 14.38 5.18 0.475 86 23.71 6.70 80 25.52 5.45 0.060
65 86 12.66 6.58 80 13.40 5.07 0.422 86 21.85 6.68 80 23.60 5.04 0.061
60 85 11.25 6.83 81 11.62 6.00 0.709 85 20.86 6.73 81 21.54 6.29 0.502
55 84 9.91 7.63 81 10.25 6.25 0.757 84 19.36 7.17 81 20.09 6.02 0.476
50 86 7.21 9.42 81 8.41 5.95 0.331 86 17.24 8.60 81 18.61 5.76 0.232
45 85 4.47 10.40 81 5.79 7.47 0.352 85 14.42 9.01 81 16.15 6.94 0.170
40 84 1.75 10.99 80 3.59 6.80 0.203 84 11.57 9.47 80 13.73 6.58 0.094
5000 Hz DPOAE levels 5000 Hz SNR analysis
70 85 14.12 8.10 82 14.30 7.37 0.883 85 23.75 7.56 82 25.00 7.17 0.276
65 85 12.37 7.57 82 12.09 8.38 0.816 85 21.32 7.18 82 21.81 7.50 0.671
60 86 10.85 7.95 82 10.84 8.72 0.991 86 19.92 7.53 82 20.60 8.09 0.572
55 85 8.78 7.99 81 9.46 7.15 0.566 85 18.07 6.98 81 19.15 5.91 0.287
50 84 5.99 9.37 82 6.47 8.89 0.735 84 15.80 7.61 82 16.54 7.91 0.539
45 85 3.22 10.48 82 4.40 9.59 0.450 85 13.46 8.52 82 14.71 8.55 0.343
40 83 −0.18 11.95 80 2.45 7.68 0.098 83 9.96 9.92 80 12.58 6.81 0.052
6000 Hz DPOAE levels 6000 Hz SNR analysis
70 86 13.56 9.39 82 14.05 7.72 0.717 86 23.99 9.39 82 25.08 7.79 0.418
65 84 12.22 8.22 80 12.53 7.62 0.801 84 21.77 7.71 80 22.51 7.38 0.534
60 86 9.02 10.01 80 10.09 7.46 0.441 86 18.92 8.74 80 19.98 7.01 0.389
55 83 6.63 11.00 81 6.85 8.48 0.885 83 16.78 9.51 81 16.94 8.00 0.905
50 84 2.36 13.19 81 4.01 8.68 0.346 84 12.78 11.43 81 14.85 7.46 0.173
45 81 −0.32 12.88 80 0.25 9.64 0.751 81 10.01 10.71 80 11.48 8.55 0.340
40 78 −4.29 13.35 73 −4.02 11.54 0.893 78 6.65 10.90 73 7.72 9.80 0.528

Table 12.

DPOAE levels – I/O analysis in male smokers and female smokers.

L2 level dB SPL Male smokers Female smokers p Male smokers Female smokers p
n mean SD n mean SD n mean SD n mean SD
1000 Hz DPOAE levels 1000 Hz SNR analysis
70 40 9.74 5.51 42 9.03 6.38 0.590 40 12.25 5.66 42 12.13 5.53 0.924
65 43 5.76 7.02 41 8.06 6.77 0.131 43 8.38 6.74 41 10.90 4.90 0.053
60 43 4.67 7.71 41 7.69 6.69 0.058 43 7.17 7.39 41 10.54 5.75 0.022
55 41 3.60 6.08 41 6.56 6.29 0.034 41 7.77 6.16 41 10.52 5.03 0.030
50 40 1.93 6.26 39 4.66 6.75 0.067 40 6.04 6.81 39 10.01 4.94 0.004
45 36 −0.69 6.72 39 2.48 7.07 0.050 36 4.43 7.16 39 7.62 5.25 0.033
40 30 −3.44 9.07 34 −1.55 10.25 0.436 30 2.15 7.46 34 4.39 8.71 0.273
1500 Hz DPOAE levels 1500 Hz SNR analysis
70 44 10.49 7.26 41 13.45 7.84 0.075 44 15.90 7.55 41 17.77 8.15 0.276
65 43 8.81 8.90 41 12.68 7.28 0.032 43 13.91 8.32 41 16.93 7.42 0.083
60 43 8.08 6.13 42 11.07 7.73 0.052 43 14.12 5.59 42 15.42 6.75 0.339
55 42 6.01 6.61 42 9.09 9.08 0.080 42 12.15 6.21 42 14.37 7.95 0.157
50 42 2.74 9.62 41 7.75 6.67 0.007 42 9.92 7.78 41 12.92 5.93 0.051
45 39 2.18 6.28 40 4.54 8.95 0.178 39 10.14 5.29 40 10.55 6.65 0.764
40 42 −1.66 8.57 34 2.10 10.57 0.099 42 6.31 7.80 34 7.94 7.86 0.370
2000 Hz DPOAE levels 2000 Hz SNR analysis
70 44 10.66 4.62 42 13.20 5.72 0.026 44 18.10 5.84 42 21.49 6.43 0.012
65 44 9.51 4.98 42 12.33 5.72 0.017 44 16.67 6.09 42 19.40 5.76 0.035
60 44 6.83 8.19 42 10.60 6.06 0.017 44 14.44 8.20 42 18.10 5.87 0.020
55 42 6.57 5.41 42 8.66 6.27 0.106 42 14.45 5.96 42 16.23 6.12 0.182
50 43 3.24 8.31 41 6.70 6.31 0.034 43 12.20 7.94 41 14.96 6.06 0.076
45 42 1.58 5.96 41 4.27 6.70 0.057 42 10.74 6.96 41 12.81 5.11 0.126
40 38 −2.09 8.18 38 2.19 6.70 0.015 38 7.10 6.77 38 10.65 5.43 0.014
3000 Hz DPOAE levels 3000 Hz SNR analysis
70 43 9.85 5.04 42 10.54 6.11 0.571 43 20.00 5.28 50 22.41 4.57 0.481
65 43 8.54 6.36 42 9.83 6.11 0.342 43 17.62 6.58 50 20.05 4.29 0.165
60 44 6.68 6.55 42 8.20 6.24 0.274 44 15.82 6.91 50 18.63 5.19 0.261
55 44 4.91 7.98 42 7.11 6.23 0.157 44 14.46 7.23 50 17.67 4.78 0.121
50 44 2.78 8.99 42 5.15 7.00 0.175 44 12.78 7.71 50 15.86 4.51 0.119
45 43 −0.87 12.06 40 1.53 10.80 0.343 43 9.27 10.39 50 13.73 7.21 0.258
40 40 −3.29 12.61 39 1.38 6.45 0.042 40 8.29 10.72 50 10.95 7.13 0.060
4000 Hz DPOAE levels 4000 Hz SNR analysis
70 44 13.07 6.77 42 14.44 5.75 0.311 44 22.68 6.93 42 24.79 6.36 0.144
65 44 11.84 7.18 42 13.52 5.85 0.239 44 21.05 7.24 42 22.70 6.01 0.253
60 43 10.61 7.37 42 11.90 6.24 0.385 43 19.72 7.49 42 22.03 5.72 0.114
55 42 9.20 8.56 42 10.61 6.60 0.401 42 18.21 7.96 42 20.50 6.15 0.145
50 44 6.09 9.99 42 8.40 8.75 0.257 44 16.17 9.46 42 18.37 7.55 0.234
45 43 3.41 11.15 42 5.55 9.59 0.346 43 13.21 10.03 42 15.65 7.75 0.213
40 42 0.84 11.43 42 2.67 10.59 0.450 42 10.51 10.06 42 12.62 8.85 0.309
5000 Hz DPOAE levels 5000 Hz SNR analysis
70 43 12.76 8.53 42 15.52 7.48 0.116 43 21.97 7.79 42 25.57 6.95 0.027
65 43 11.14 7.53 42 13.63 7.49 0.130 43 20.09 7.50 42 22.58 6.69 0.110
60 44 9.43 8.43 42 12.35 7.21 0.087 44 18.12 8.00 42 21.80 6.58 0.022
55 43 7.67 8.23 42 9.92 7.66 0.195 43 16.52 7.40 42 19.66 6.22 0.037
50 43 4.60 9.43 41 7.44 9.21 0.166 43 14.65 7.89 41 17.00 7.20 0.158
45 43 2.43 10.38 42 4.03 10.65 0.487 43 12.44 8.57 42 14.50 8.44 0.270
40 42 −1.00 11.57 41 0.66 12.41 0.531 42 9.18 9.45 41 10.76 10.43 0.470
6000 Hz DPOAE levels 6000 Hz SNR analysis
70 44 12.35 10.25 42 14.84 8.32 0.219 44 22.65 10.64 42 25.40 7.74 0.174
65 42 11.75 8.10 42 12.69 8.41 0.600 42 21.18 7.72 42 22.36 7.74 0.483
60 44 7.71 10.69 42 10.40 9.16 0.214 44 17.61 9.69 42 20.28 7.49 0.156
55 43 5.73 10.40 40 7.59 11.66 0.446 43 15.62 9.31 40 18.03 9.68 0.252
50 43 1.76 12.21 41 2.99 14.27 0.671 43 12.29 10.90 41 13.30 12.07 0.690
45 42 −2.10 13.28 39 1.59 12.31 0.197 42 8.59 11.32 39 11.55 9.94 0.214
40 38 −5.92 13.34 40 −2.75 13.34 0.297 38 5.13 11.00 40 8.09 10.74 0.232

Table 13.

DPOAE levels – I/O analysis in male non-smokers and female non-smokers.

L2 level dB SPL Male non-smokers Female non-smokers p Male non-smokers Female non-smokers p
n mean SD n mean SD n mean SD n mean SD
1000 Hz DPOAE levels 1000 Hz SNR analysis
70 31 9.83 8.57 49 9.57 5.27 0.880 31 12.63 7.85 49 13.33 5.81 0.320
65 32 8.21 5.87 49 6.73 5.83 0.269 32 11.06 7.22 49 10.73 5.57 0.880
60 29 8.33 4.62 49 6.46 5.63 0.115 29 11.76 5.33 49 10.60 6.02 0.957
55 31 5.87 8.67 46 5.13 5.94 0.677 31 9.38 8.29 46 10.12 4.60 0.695
50 30 5.32 6.36 45 2.72 8.19 0.127 30 10.01 5.25 45 8.63 8.20 0.362
45 30 3.34 7.00 42 2.40 5.44 0.543 30 8.47 6.32 42 8.41 5.54 0.513
40 26 1.72 6.14 42 −2.25 9.33 0.038 26 6.82 6.45 42 4.77 8.11 0.844
1500 Hz DPOAE levels 1500 Hz SNR analysis
70 32 13.85 5.59 49 13.26 5.40 0.637 32 20.27 7.03 49 20.45 6.05 0.903
65 32 12.62 5.65 48 12.27 5.10 0.779 32 18.24 6.16 48 18.13 5.88 0.936
60 32 10.89 6.76 47 11.03 5.28 0.923 32 16.56 6.29 47 16.87 5.84 0.824
55 31 9.36 7.33 49 8.01 8.82 0.460 31 15.29 7.75 49 14.21 7.82 0.549
50 31 7.14 8.11 49 6.05 7.18 0.541 31 13.34 7.22 49 12.65 6.69 0.670
45 30 6.17 6.96 49 4.20 7.44 0.238 30 12.81 6.40 49 11.62 7.12 0.446
40 29 1.99 10.67 49 1.72 7.26 0.905 29 9.46 9.80 49 10.05 6.46 0.775
2000 Hz DPOAE levels 2000 Hz SNR analysis
70 31 13.19 6.17 50 11.38 5.47 0.185 31 22.45 6.30 50 20.54 6.22 0.188
65 31 12.13 6.36 50 10.68 5.44 0.296 31 20.03 6.69 50 19.42 5.81 0.676
60 30 11.11 7.14 50 9.59 5.50 0.320 30 19.36 7.74 50 18.15 6.22 0.471
55 31 9.12 7.52 50 7.68 5.50 0.361 31 18.53 7.56 50 16.72 5.63 0.255
50 30 6.76 10.01 49 5.58 5.82 0.560 30 15.22 10.43 49 14.91 5.22 0.881
45 31 4.22 8.15 49 2.03 8.98 0.264 31 13.34 7.77 49 12.19 7.80 0.522
40 31 −0.37 10.73 48 −1.61 10.26 0.611 31 9.02 10.26 48 8.76 9.32 0.911
3000 Hz DPOAE levels 3000 Hz SNR analysis
70 31 11.26 7.17 50 10.97 4.58 0.844 31 21.63 7.99 50 22.41 4.57 0.624
65 31 9.72 8.91 50 10.07 4.50 0.841 31 19.43 9.88 50 20.05 4.29 0.739
60 31 8.86 6.90 50 8.58 5.15 0.846 31 18.54 6.83 50 18.63 5.19 0.949
55 32 6.89 9.75 50 7.41 5.22 0.783 32 16.47 10.11 50 17.67 4.78 0.534
50 32 5.70 7.58 50 5.61 5.48 0.953 32 15.81 7.73 50 15.86 4.51 0.974
45 32 3.32 7.56 50 2.46 7.84 0.623 32 13.82 8.26 50 13.73 7.21 0.960
40 30 2.34 5.53 50 −0.37 8.02 0.078 30 12.83 5.94 50 10.95 7.13 0.208
4000 Hz DPOAE levels 4000 Hz SNR analysis
70 30 14.84 5.11 50 14.11 5.26 0.544 30 25.95 5.40 50 25.26 5.52 0.585
65 30 13.70 5.12 50 13.22 5.08 0.684 30 23.71 4.50 50 23.53 5.37 0.875
60 31 11.23 7.24 50 11.87 5.15 0.672 31 20.81 7.77 50 22.00 5.21 0.453
55 31 9.94 7.31 50 10.43 5.56 0.749 31 18.97 7.30 50 20.79 5.02 0.229
50 31 8.09 6.64 50 8.61 5.54 0.716 31 17.69 6.83 50 19.18 4.98 0.298
45 31 5.62 7.40 50 5.89 7.59 0.875 31 15.45 7.62 50 16.58 6.54 0.500
40 32 2.76 7.67 48 4.14 6.17 0.397 32 12.48 7.47 48 14.55 5.84 0.191
5000 Hz DPOAE levels 5000 Hz SNR analysis
70 32 13.56 8.61 50 14.77 6.51 0.497 32 24.26 8.35 50 25.47 6.35 0.488
65 32 11.25 9.94 50 12.62 7.27 0.504 32 20.91 9.20 50 22.38 6.20 0.428
60 32 10.38 8.61 50 11.14 8.86 0.702 32 19.69 8.46 50 21.18 7.87 0.425
55 31 9.47 6.42 50 9.45 7.64 0.989 31 18.73 5.27 50 19.41 6.31 0.603
50 32 5.48 9.93 50 7.10 8.19 0.443 32 15.65 9.17 50 17.11 7.03 0.447
45 32 2.81 11.40 50 5.42 8.20 0.266 32 12.96 10.75 50 15.84 6.67 0.182
40 31 1.00 8.67 49 3.36 6.92 0.207 31 10.94 7.08 49 13.62 6.50 0.093
6000 Hz DPOAE levels 6000 Hz SNR analysis
70 32 14.22 8.87 50 13.93 6.97 0.878 32 24.90 8.76 50 25.19 7.20 0.875
65 30 13.36 8.64 50 12.04 6.98 0.480 30 22.99 8.57 50 22.22 6.65 0.675
60 30 11.31 6.75 50 9.35 7.83 0.241 30 20.69 6.87 50 19.56 7.13 0.485
55 32 6.76 10.18 49 6.91 7.27 0.944 32 15.87 10.15 49 17.64 6.23 0.381
50 32 4.40 8.46 49 3.75 8.90 0.743 32 14.60 8.04 49 15.01 7.14 0.816
45 32 −0.07 9.98 48 0.46 9.51 0.813 32 10.48 9.44 48 12.14 7.94 0.418
40 31 −4.95 12.25 42 −3.34 11.09 0.566 31 6.37 10.34 42 8.71 9.39 0.323

Table 14.

DPOAE levels – I/O analysis in male smokers and male non-smokers.

L2 level dB SPL Male smokers Male non-smokers p Male smokers Male non-smokers p
n mean SD n mean SD n mean SD n mean SD
1000 Hz DPOAE levels 1000 Hz SNR analysis
70 40 9.74 5.51 31 9.83 8.57 0.956 40 12.25 5.66 31 12.63 7.85 0.814
65 43 5.76 7.02 32 8.21 5.87 0.114 43 8.38 6.74 32 11.06 7.22 0.103
60 43 4.67 7.71 29 8.33 4.62 0.025 43 7.17 7.39 29 11.76 5.33 0.005
55 41 3.60 6.08 31 5.87 8.67 0.195 41 7.77 6.16 31 9.38 8.29 0.346
50 40 1.93 6.26 30 5.32 6.36 0.029 40 6.04 6.81 30 10.01 5.25 0.010
45 36 −0.69 6.72 30 3.34 7.00 0.020 36 4.43 7.16 30 8.47 6.32 0.019
40 30 −3.44 9.07 26 1.72 6.14 0.017 30 2.15 7.46 26 6.82 6.45 0.016
1500 Hz DPOAE levels 1500 Hz SNR analysis
70 44 10.49 7.26 32 13.85 5.59 0.032 44 15.90 7.55 32 20.27 7.03 0.012
65 43 8.81 8.90 32 12.62 5.65 0.037 43 13.91 8.32 32 18.24 6.16 0.016
60 43 8.08 6.13 32 10.89 6.76 0.064 43 14.12 5.59 32 16.56 6.29 0.081
55 42 6.01 6.61 31 9.36 7.33 0.045 42 12.15 6.21 31 15.29 7.75 0.059
50 42 2.74 9.62 31 7.14 8.11 0.043 42 9.92 7.78 31 13.34 7.22 0.060
45 39 2.18 6.28 30 6.17 6.96 0.015 39 10.14 5.29 30 12.81 6.40 0.062
40 42 −1.66 8.57 29 1.99 10.67 0.115 42 6.31 7.80 29 9.46 9.80 0.137
2000 Hz DPOAE levels 2000 Hz SNR analysis
70 44 10.66 4.62 31 13.19 6.17 0.045 44 18.10 5.84 31 22.45 6.30 0.003
65 44 9.51 4.98 31 12.13 6.36 0.049 44 16.67 6.09 31 20.03 6.69 0.027
60 44 6.83 8.19 30 11.11 7.14 0.023 44 14.44 8.20 30 19.36 7.74 0.012
55 42 6.57 5.41 31 9.12 7.52 0.097 42 14.45 5.96 31 18.53 7.56 0.012
50 43 3.24 8.31 30 6.76 10.01 0.106 43 12.20 7.94 30 15.22 10.43 0.165
45 42 1.58 5.96 31 4.22 8.15 0.113 42 10.74 6.96 31 13.34 7.77 0.139
40 38 −2.09 8.18 31 −0.37 10.73 0.454 38 7.10 6.77 31 9.02 10.26 0.355
3000 Hz DPOAE levels 3000 Hz SNR analysis
70 43 9.85 5.04 31 11.26 7.17 0.325 43 20.00 5.28 31 21.63 7.99 0.293
65 43 8.54 6.36 31 9.72 8.91 0.509 43 17.62 6.58 31 19.43 9.88 0.349
60 44 6.68 6.55 31 8.86 6.90 0.169 44 15.82 6.91 31 18.54 6.83 0.095
55 44 4.91 7.98 32 6.89 9.75 0.335 44 14.46 7.23 32 16.47 10.11 0.315
50 44 2.78 8.99 32 5.70 7.58 0.139 44 12.78 7.71 32 15.81 7.73 0.095
45 43 −0.87 12.06 32 3.32 7.56 0.089 43 9.27 10.39 32 13.82 8.26 0.045
40 40 −3.29 12.61 30 2.34 5.53 0.025 40 8.29 10.72 30 12.83 5.94 0.041
4000 Hz DPOAE levels 4000 Hz SNR analysis
70 44 13.07 6.77 30 14.84 5.11 0.228 44 22.68 6.93 30 25.95 5.40 0.033
65 44 11.84 7.18 30 13.70 5.12 0.227 44 21.05 7.24 30 23.71 4.50 0.078
60 43 10.61 7.37 31 11.23 7.24 0.720 43 19.72 7.49 31 20.81 7.77 0.547
55 42 9.20 8.56 31 9.94 7.31 0.700 42 18.21 7.96 31 18.97 7.30 0.678
50 44 6.09 9.99 31 8.09 6.64 0.333 44 16.17 9.46 31 17.69 6.83 0.445
45 43 3.41 11.15 31 5.62 7.40 0.341 43 13.21 10.03 31 15.45 7.62 0.300
40 42 0.84 11.43 32 2.76 7.67 0.415 42 10.51 10.06 32 12.48 7.47 0.356
5000 Hz DPOAE levels 5000 Hz SNR analysis
70 43 12.76 8.53 32 13.56 8.61 0.691 43 21.97 7.79 32 24.26 8.35 0.227
65 43 11.14 7.53 32 11.25 9.94 0.957 43 20.09 7.50 32 20.91 9.20 0.675
60 44 9.43 8.43 32 10.38 8.61 0.631 44 18.12 8.00 32 19.69 8.46 0.413
55 43 7.67 8.23 31 9.47 6.42 0.313 43 16.52 7.40 31 18.73 5.27 0.160
50 43 4.60 9.43 32 5.48 9.93 0.699 43 14.65 7.89 32 15.65 9.17 0.614
45 43 2.43 10.38 32 2.81 11.40 0.884 43 12.44 8.57 32 12.96 10.75 0.817
40 42 −1.00 11.57 31 1.00 8.67 0.421 42 9.18 9.45 31 10.94 7.08 0.387
6000 Hz DPOAE levels 6000 Hz SNR analysis
70 44 12.35 10.25 32 14.22 8.87 0.408 44 22.65 10.64 32 24.90 8.76 0.332
65 42 11.75 8.10 30 13.36 8.64 0.420 42 21.18 7.72 30 22.99 8.57 0.352
60 44 7.71 10.69 30 11.31 6.75 0.107 44 17.61 9.69 30 20.69 6.87 0.138
55 43 5.73 10.40 32 6.76 10.18 0.670 43 15.62 9.31 32 15.87 10.15 0.911
50 43 1.76 12.21 32 4.40 8.46 0.297 43 12.29 10.90 32 14.60 8.04 0.316
45 42 −2.10 13.28 32 −0.07 9.98 0.472 42 8.59 11.32 32 10.48 9.44 0.446
40 38 −5.92 13.34 31 −4.95 12.25 0.754 38 5.13 11.00 31 6.37 10.34 0.634

Table 15.

DPOAE levels – I/O analysis in female smokers and female non-smokers.

L2 level dB SPL Female smokers Female non-smokers p Female smokers Female non-smokers p
n mean SD n mean SD n mean SD n mean SD
1000 Hz DPOAE levels 1000 Hz SNR analysis
70 42 9.03 6.38 49 9.57 5.27 0.658 42 12.13 5.53 49 13.33 5.81 0.320
65 41 8.06 6.77 49 6.73 5.83 0.320 41 10.90 4.90 49 10.73 5.57 0.880
60 41 7.69 6.69 49 6.46 5.63 0.346 41 10.54 5.75 49 10.60 6.02 0.957
55 41 6.56 6.29 46 5.13 5.94 0.279 41 10.52 5.03 46 10.12 4.60 0.695
50 39 4.66 6.75 45 2.72 8.19 0.244 39 10.01 4.94 45 8.63 8.20 0.362
45 39 2.48 7.07 42 2.40 5.44 0.952 39 7.62 5.25 42 8.41 5.54 0.513
40 34 −1.55 10.25 42 −2.25 9.33 0.757 34 4.39 8.71 42 4.77 8.11 0.844
1500 Hz DPOAE levels 1500 Hz SNR analysis
70 41 13.45 7.84 49 13.26 5.40 0.889 41 17.77 8.15 49 20.45 6.05 0.077
65 41 12.68 7.28 48 12.27 5.10 0.754 41 16.93 7.42 48 18.13 5.88 0.399
60 42 11.07 7.73 47 11.03 5.28 0.974 42 15.42 6.75 47 16.87 5.84 0.279
55 42 9.09 9.08 49 8.01 8.82 0.566 42 14.37 7.95 49 14.21 7.82 0.924
50 41 7.75 6.67 49 6.05 7.18 0.251 41 12.92 5.93 49 12.65 6.69 0.841
45 40 4.54 8.95 49 4.20 7.44 0.845 40 10.55 6.65 49 11.62 7.12 0.468
40 34 2.10 10.57 49 1.72 7.26 0.849 34 7.94 7.86 49 10.05 6.46 0.184
2000 Hz DPOAE levels 2000 Hz SNR analysis
70 42 13.20 5.72 50 11.38 5.47 0.123 42 21.49 6.43 50 20.54 6.22 0.475
65 42 12.33 5.72 50 10.68 5.44 0.160 42 19.40 5.76 50 19.42 5.81 0.988
60 42 10.60 6.06 50 9.59 5.50 0.406 42 18.10 5.87 50 18.15 6.22 0.968
55 42 8.66 6.27 50 7.68 5.50 0.425 42 16.23 6.12 50 16.72 5.63 0.691
50 41 6.70 6.31 49 5.58 5.82 0.383 41 14.96 6.06 49 14.91 5.22 0.966
45 41 4.27 6.70 49 2.03 8.98 0.192 41 12.81 5.11 49 12.19 7.80 0.659
40 38 2.19 6.70 48 −1.61 10.26 0.051 38 10.65 5.43 48 8.76 9.32 0.270
3000 Hz DPOAE levels 3000 Hz SNR analysis
70 42 10.54 6.11 50 10.97 4.58 0.701 42 20.90 6.41 50 22.41 4.57 0.192
65 42 9.83 6.11 50 10.07 4.50 0.833 42 19.47 5.56 50 20.05 4.29 0.572
60 42 8.20 6.24 50 8.58 5.15 0.747 42 17.40 6.10 50 18.63 5.19 0.299
55 42 7.11 6.23 50 7.41 5.22 0.803 42 16.70 6.02 50 17.67 4.78 0.394
50 42 5.15 7.00 50 5.61 5.48 0.723 42 15.05 5.48 50 15.86 4.51 0.438
45 40 1.53 10.80 50 2.46 7.84 0.637 40 11.67 8.74 50 13.73 7.21 0.224
40 39 1.38 6.45 50 −0.37 8.02 0.270 39 11.89 5.03 50 10.95 7.13 0.484
4000 Hz DPOAE levels 4000 Hz SNR analysis
70 42 14.44 5.75 50 14.11 5.26 0.771 42 24.79 6.36 50 25.26 5.52 0.707
65 42 13.52 5.85 50 13.22 5.08 0.794 42 22.70 6.01 50 23.53 5.37 0.483
60 42 11.90 6.24 50 11.87 5.15 0.974 42 22.03 5.72 50 22.00 5.21 0.980
55 42 10.61 6.60 50 10.43 5.56 0.889 42 20.50 6.15 50 20.79 5.02 0.805
50 42 8.40 8.75 50 8.61 5.54 0.886 42 18.37 7.55 50 19.18 4.98 0.540
45 42 5.55 9.59 50 5.89 7.59 0.850 42 15.65 7.75 50 16.58 6.54 0.537
40 42 2.67 10.59 48 4.14 6.17 0.414 42 12.62 8.85 48 14.55 5.84 0.220
5000 Hz DPOAE levels 5000 Hz SNR analysis
70 42 15.52 7.48 50 14.77 6.51 0.611 42 25.57 6.95 50 25.47 6.35 0.942
65 42 13.63 7.49 50 12.62 7.27 0.513 42 22.58 6.69 50 22.38 6.20 0.883
60 42 12.35 7.21 50 11.14 8.86 0.478 42 21.80 6.58 50 21.18 7.87 0.688
55 42 9.92 7.66 50 9.45 7.64 0.770 42 19.66 6.22 50 19.41 6.31 0.848
50 41 7.44 9.21 50 7.10 8.19 0.853 41 17.00 7.20 50 17.11 7.03 0.942
45 42 4.03 10.65 50 5.42 8.20 0.480 42 14.50 8.44 50 15.84 6.67 0.397
40 41 0.66 12.41 49 3.36 6.92 0.196 41 10.76 10.43 49 13.62 6.50 0.117
6000 Hz DPOAE levels 6000 Hz SNR analysis
70 42 14.84 8.32 50 13.93 6.97 0.573 42 25.40 7.74 50 25.19 7.20 0.894
65 42 12.69 8.41 50 12.04 6.98 0.683 42 22.36 7.74 50 22.22 6.65 0.921
60 42 10.40 9.16 50 9.35 7.83 0.557 42 20.28 7.49 50 19.56 7.13 0.638
55 40 7.59 11.66 49 6.91 7.27 0.735 40 18.03 9.68 49 17.64 6.23 0.821
50 41 2.99 14.27 49 3.75 8.90 0.759 41 13.30 12.07 49 15.01 7.14 0.406
45 39 1.59 12.31 48 0.46 9.51 0.629 39 11.55 9.94 48 12.14 7.94 0.760
40 40 −2.75 13.34 42 −3.34 11.09 0.828 40 8.09 10.74 42 8.71 9.39 0.781

Altogether, the aforementioned data suggest that smoking impairs the OHC function in men, but not in women.

Spontaneous otoacoustic emissions

The results of SOAE analysis were consistent with the abovementioned data on DPOAE levels in an I/O function. Male smokers were at greater risk of toxic OHC impairment than female smokers. SOAEs were observed in 4.3% and 25% of male smokers and non-smokers, respectively, and in 47.6% and 60.5% of female smokers and non-smokers, respectively. This clearly shows that men are more susceptible to smoking-induced hearing impairment.

Discussion

The effects of isolated exposure to tobacco smoke are extremely difficult to determine because smokers are frequently co-exposed to other ototoxic factors, especially in an occupational setting [1820]. Moreover, the differences in male and female physiology should be considered; namely, the potential protective effect of hormonal factors on the female hearing organ [21,22]. Finally, the accurate evaluation of the hearing effects requires a group of individuals with sufficiently long and extensive exposure to the components of tobacco smoke. Furthermore, the selection of an appropriate method for hearing examination is an important issue since not every test is suitable for detection of changes at a subclinical level. Evaluation of otoacoustic emissions is an objective and highly sensitive method for hearing assessment [1618,23,24]. The sensitivity of this test can be improved by the use of various intensities of L1 and L2 stimuli, as well as by the implementation of an input/output function [2426].

The smokers and non-smokers participating in our study did not differ significantly in terms of their results of PTA at a 250–20 000 Hz frequency range. However, despite the lack of statistically significant differences, the hearing threshold of smokers was slightly higher than in non-smokers. This observation is consistent with the data published recently by Negley et al. [26]. Although the hearing threshold at a standard spectrum did not exceed 25 dB HL in any of the subjects participating in this study, the smokers presented with a 2–10 dB higher hearing thresholds than the controls. However, the smokers and non-smokers did not differ significantly in terms of their hearing thresholds at high frequencies [26]. In contrast, Paschoal and Azevedo [27] found significant differences in the audiometric hearing thresholds of smokers and non-smokers at 8 kHz, 12.5 kHz, and 14 kHz. Also, Oliveira and Lima [28] showed that the individuals who smoked for at least 5 years presented with significantly higher (albeit within a normal limit) hearing thresholds at a standard spectrum and at high frequencies than the subjects who never smoked. However, this study involved a relatively small sample of smokers (n=30), and its authors did not provide information about the daily number of cigarettes smoked in this group [28]. Basar and Belgin [29] examined 30 individuals with a 10-year history of smoking at least 1 package per day and 20 non-smoking controls, and found that the former presented with significantly higher hearing thresholds solely at 16 kHz and 18 kHz. Sousa et al. [30] analyzed the exposure of 625 volunteers to various risk factors of hearing impairment. Neither PTA nor speech audiometry confirmed the role of tobacco smoking as a risk factor for this condition [30]. The influence of tobacco smoking and noise on hearing, examined by means of tone audiometry at a standard spectrum, was also analyzed by Pouryaghoub et al. [20]; they found that a group of 206 smokers was characterized by significantly higher hearing threshold at 4 kHz when compared to 206 non-smoking controls.

Aside from smoking, the hearing impairment documented in some of our participants might be related to their sex, age (up to 67 years), and/or exposure to noise [20]. An important study analyzing the effect of sex on the auditory consequences of smoking was conducted by Uchida et al. [31]. They found that the results of PTA at 4000 Hz were significantly worse in male smokers than in male non-smokers, but a similar phenomenon was not observed in the case of female smokers and non-smokers [31]. Nomura et al. [32] conducted a meta-analysis of 15 studies published between 1966 and 2003, in order to determine the effects of cigarette smoking on the results of PTA. They documented the unfavorable effect of smoking in 9 out of the 15 analyzed studies; the lack of such an association in the remaining studies suggests that the relationship between smoking and hearing impairment is still not completely understood [32].

Previous research on click-evoked otoacoustic emissions [27,33,34] showed that smokers present with lower CEOAE levels than non-smokers. Paschoal and Azevedo [27] did not observe CEOAEs in 13.9% and 2.8% of smokers and non-smokers, respectively (p=0.016). The levels of CEOAEs do not seem to be modulated by the age of smokers [34]. Interestingly, a study of CEOAEs in newborns whose mothers smoked during pregnancy demonstrated not only the functional impairment of sound perception, but also the structural abnormalities of the hearing organ [33]. In our study, male smokers presented with significantly lower CEOAE levels than male non-smokers and female smokers. To the best of our knowledge, this was the first study to demonstrate sex-specific differences in smokers’ CEOAE levels.

Apart from CEOAEs, we evaluated otoacoustic emissions as a DP-gram function. Negley et al. [26] analyzed the DP-grams obtained using high (L1=L2=70 dB SPL) and moderate (L1=65 dB SPL, L2=50 dB SPL) intensity of stimulation, and showed that smokers presented with significantly lower DPOAE levels at all frequencies. In contrast, we used L1=71 dB SPL and L2 = 60 dB SPL stimulus intensities and did not document significant differences in DPOAEs levels of smokers and non-smokers on most comparisons, also when adjusted for sex. Torre et al. [35] did not find a significant effect of smoking on DPOAE levels (2.3–8.0 kHz), but their results might have been confounded by selection bias, since it included subjects who smoked no longer than for 1 year, which might be an insufficient exposure to tobacco smoke [35]. Furthermore, we showed that compared to male non-smokers, male long-term smokers presented with significantly lower DPOAE levels at 1685 Hz; this suggests a sex-specific effect of smoking on DPOAEs.

The results of our analysis of DPOAEs in an input/output function, being a highly sensitive test for the active and passive mechanisms of the cochlea, are consistent with the data published by Negley et al. [26]. These authors showed that a gradual increase in the stimulation intensity (from 20 dB SPL to 80 dB SPL, at 10-dB intervals) is reflected by a f2 frequency-specific increase in the I/O emission, by 10 dB, 8 dB, and 5 dB for 2 kHz, 4 kHz, and 8 kHz, respectively [26]. In our study, statistically significant differences between smokers and non-smokers were observed at 1 kHz, 1.5 kHz, 2 kHz, and 3 kHz. Moreover, we found significant differences between male smokers and male non-smokers at 1 kHz, 1.5 kHz, 2 kHz, 3 kHz, and 4 kHz, as well as between male and female smokers at 1 kHz, 2 kHz, and 5 kHz. Altogether, these findings suggest that smoking exerts particularly unfavorable effects on the cochlear OHC in men, but not in women.

Importantly, we showed that the incidence SOAEs in smokers was significantly lower than in non-smokers. This new observation requires verification in future studies.

To the best of our knowledge, our study is the first to demonstrate sex-specific differences in CEOAE, DPOAE, and OAE responses of smokers. Using an objective method for otoacoustic emission analysis, we showed that the smoking-related alterations were more pronounced in men than in women. These sex-specific differences in otoacoustic emission levels might reflect the influence of genetic, hormonal, behavioral, and/or environmental factors.

Previous studies documented evident sex-specific differences in the CEOAE levels of infants and children. Cassidy and Ditty [36] showed that compared to male newborns, female newborns present with significantly higher CEOAE levels at 1.6 kHz, 2.4 kHz, 3.2 kHz, and 4.0 kHz. Also, Aidan et al. [37] demonstrated that mean CEOAE levels in female neonates are higher than in male neonates (22.1 dB SPL vs. 21.4 dB SPL). Interestingly, the same study documented significant differences in the CEOAE levels recorded in the right and left ear (22.4 dB SPL vs. 21 dB SPL) [37]. In another study, 12-year-old girls were shown to present with significantly higher CEOAE levels than their male peers [38]. However, in contrast to Aidan et al. [37], the authors of this study did not observe a bilateral asymmetry in CEOAE levels [38]. Although we did not reveal sex-specific differences in the otoacoustic emission levels of non-smokers, it cannot be excluded that men present with a genetically determined (i.e., sex hormone-independent) greater susceptibility of cochlear OHCs to the ototoxic components of tobacco smoke.

The results of experimental studies point to a potential protective effect of female sex hormones as an explanation of sex-specific differences in hearing. Estrogens, 17α-estradiol, 17β-estradiol, estrone, and estriol were shown to protect against gentamicin-induced outer hair cell death; the effect of 17β-estradiol is mediated by estrogen receptor (ER) [39]. Interestingly, the expression of estrogen receptors ERα and ERβ in the inner ear (i.e., in the nuclei of stria vascularis, outer and inner hair cells, spiral ganglion cells, vestibular ganglion cells, and vestibular dark cells) is known to decrease with age [40]. These findings are consistent with the results of clinical studies. For example, Kilicdag et al. [21] demonstrated that estrogen therapy may protect against hearing loss in aging postmenopausal women. Taking this evidence into account, it can be hypothesized that female sex hormones may also protect against tobacco smoke-induced hearing impairment.

Behavioral factors should also be considered as a potential cause of sex-specific differences in susceptibility to tobacco smoke-related hearing loss. Men not only smoke more, but also use stronger cigarettes, as well as other stimulants [4143]. Our study included 21 women and 22 men, who smoked at least 15 cigarettes per day for at least 7 years. We did not compare, however, the total number of cigarettes smoked by the female and male participants. Consequently, our male smokers might be exposed to tobacco smoke more often and for a longer period of time than female smokers. Finally, the influence of environmental chemical ototoxins should be taken into account as a confounding factor resulting in greater impairment of hearing in our male smokers [44].

To summarize, tobacco smoke likely induces an array of subclinical changes in the organ of hearing, especially in males. Therefore, appropriate strategies preventing resultant hearing loss should be implemented before it will manifest clinically and impair patient functioning. These strategies should be adjusted for these documented sex-specific differences in susceptibility to tobacco smoke-induced hearing impairment.

Conclusions

This study showed that smoking induces an array of subclinical changes in the organ of hearing. Specifically, while it does not modulate the hearing threshold determined with PTA at low, moderate, and high frequencies, it causes a significant decrease in OAE levels, but only in males. Furthermore, smoking impairs the active and passive mechanisms of male cochlea.

Footnotes

Disclaimers

No conflicts of interest to be noted. No relationships with industry to be noted.

Source of support: Self-financing

References

  • 1.Howard G, Wagenknecht LE, Burke GL, et al. Cigarette smoking and progression of atherosclerosis: The Atherosclerosis Risk in Communities (ARIC) Study. JAMA. 1998;279:119–24. doi: 10.1001/jama.279.2.119. [DOI] [PubMed] [Google Scholar]
  • 2.Puranik R, Celermajer DS. Smoking and endothelial function. Prog Cardiovasc Dis. 2003;45:443–58. doi: 10.1053/pcad.2003.YPCAD13. [DOI] [PubMed] [Google Scholar]
  • 3.Lloyd-Jones D, Adams R, Carnethon M, et al. Heart disease and stroke statistics – 2009 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2009;119:e21–181. doi: 10.1161/CIRCULATIONAHA.108.191261. [DOI] [PubMed] [Google Scholar]
  • 4.Czapiński J. Nikotynizm w Polsce Raport dla. World Health Organization; 2011. [in Polish] [Google Scholar]
  • 5.Lowe GD, Drummond MM, Forbes CD, Barbenel JC. The effects of age and cigarette-smoking on blood and plasma viscosity in men. Scott Med J. 1980;25:13–17. doi: 10.1177/003693308002500103. [DOI] [PubMed] [Google Scholar]
  • 6.Browning GG, Gatehouse S, Lowe GD. Blood viscosity as a factor in sensorineural hearing impairment. Lancet. 1986;1:121–23. doi: 10.1016/s0140-6736(86)92261-0. [DOI] [PubMed] [Google Scholar]
  • 7.Fechter LD, Thorne PR, Nuttall AL. Effects of carbon monoxide on cochlear electrophysiology and blood flow. Hear Res. 1987;27:37–45. doi: 10.1016/0378-5955(87)90024-4. [DOI] [PubMed] [Google Scholar]
  • 8.Prockop LD, Chichkova RI. Carbon monoxide intoxication: an updated review. J Neurol Sci. 2007;262:122–30. doi: 10.1016/j.jns.2007.06.037. [DOI] [PubMed] [Google Scholar]
  • 9.Muhammad-Kah R, Liang Q, Frost-Pineda K, et al. Factors affecting exposure to nicotine and carbon monoxide in adult cigarette smokers. Regul Toxicol Pharmacol. 2011;61:129–36. doi: 10.1016/j.yrtph.2011.07.003. [DOI] [PubMed] [Google Scholar]
  • 10.Sokolova-Djokic L, Milosevic S, Skrbic R, et al. Pulse carboxyhemoglobin-oximetry and cigarette smoking. J BUON. 2011;16:170–73. [PubMed] [Google Scholar]
  • 11.Morley BJ. Nicotinic cholinergic intercellular communication: Implications for the developing auditory system. Hear Res. 2005;206:74–88. doi: 10.1016/j.heares.2005.02.012. [DOI] [PubMed] [Google Scholar]
  • 12.Lustig LR. Nicotinic acetylcholine receptor structure and function in the efferent auditory system. Anat Rec A Discov Mol Cell Evol Biol. 2006;288:424–34. doi: 10.1002/ar.a.20302. [DOI] [PubMed] [Google Scholar]
  • 13.Derekoy FS, Dundar Y, Aslan R, Cangal A. Influence of noise exposure on antioxidant system and TEOAEs in rabbits. Eur Arch Otorhinolaryngol. 2001;258:518–22. doi: 10.1007/s004050100388. [DOI] [PubMed] [Google Scholar]
  • 14.Fechter LD, Chen GD, Rao D. Chemical asphyxiants and noise. Noise Health. 2002;4:49–61. [PubMed] [Google Scholar]
  • 15.Yamashita D, Jiang HY, Schacht J, Miller JM. Delayed production of free radicals following noise exposure. Brain Res. 2004;1019:201–9. doi: 10.1016/j.brainres.2004.05.104. [DOI] [PubMed] [Google Scholar]
  • 16.Lisowska G, Namyslowski G, Orecka B, Misiolek M. Influence of aging on medial olivocochlear system function. Clin Interv Aging. 2014;9:901–14. doi: 10.2147/CIA.S61934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Kemp DT. Otoacoustic emissions, their origin in cochlear function, and use. Br Med Bull. 2002;63:223–41. doi: 10.1093/bmb/63.1.223. [DOI] [PubMed] [Google Scholar]
  • 18.Nowak J, Bilski B. Factors modifying noise-induced hearing loss. Med Pr. 2003;54:81–86. [PubMed] [Google Scholar]
  • 19.Nomura K, Nakao M, Yano E. Hearing loss associated with smoking and occupational noise exposure in a Japanese metal working company. Int Arch Occup Environ Health. 2005;78:178–84. doi: 10.1007/s00420-005-0604-z. [DOI] [PubMed] [Google Scholar]
  • 20.Pouryaghoub G, Mehrdad R, Mohammadi S. Interaction of smoking and occupational noise exposure on hearing loss: A cross-sectional study. BMC Public Health. 2007;7:137. doi: 10.1186/1471-2458-7-137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Kilicdag EB, Yavuz H, Bagis T, et al. Effects of estrogen therapy on hearing in postmenopausal women. Am J Obstet Gynecol. 2004;190:77–82. doi: 10.1016/j.ajog.2003.06.001. [DOI] [PubMed] [Google Scholar]
  • 22.Meltser I, Tahera Y, Simpson E, et al. Estrogen receptor beta protects against acoustic trauma in mice. J Clin Invest. 2008;118:1563–70. doi: 10.1172/JCI32796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Kemp DT, Ryan S, Bray P. A guide to the effective use of otoacoustic emissions. Ear Hear. 1990;11:93–105. doi: 10.1097/00003446-199004000-00004. [DOI] [PubMed] [Google Scholar]
  • 24.Gorga MP, Neely ST, Dorn PA, Hoover BM. Further efforts to predict pure-tone thresholds from distortion product otoacoustic emission input/output functions. J Acoust Soc Am. 2003;113:3275–84. doi: 10.1121/1.1570433. [DOI] [PubMed] [Google Scholar]
  • 25.Shaffer LA, Withnell RH, Dhar S, et al. Sources and mechanisms of DPOAE generation: Implications for the prediction of auditory sensitivity. Ear Hear. 2003;24:367–79. doi: 10.1097/01.AUD.0000090439.16438.9F. [DOI] [PubMed] [Google Scholar]
  • 26.Negley C, Katbamna B, Crumpton T, Lawson GD. Effects of cigarette smoking on distortion product otoacoustic emissions. J Am Acad Audiol. 2007;18:665–74. doi: 10.3766/jaaa.18.8.4. [DOI] [PubMed] [Google Scholar]
  • 27.Paschoal CP, Azevedo MF. Cigarette smoking as a risk factor for auditory problems. Braz J Otorhinolaryngol. 2009;75:893–902. doi: 10.1016/S1808-8694(15)30556-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Oliveira DC, Lima MA. Low and high frequency tonal threshold audiometry: Comparing hearing thresholds between smokers and non-smokers. Braz J Otorhinolaryngol. 2009;75:738–44. doi: 10.1016/S1808-8694(15)30527-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Basar F, Belgin E. Evaluation of high frequency hearing thresholds in smokers. Kulak Burun Bogaz Ihtis Derg. 2008;18:19–23. [PubMed] [Google Scholar]
  • 30.Sousa CS, Castro N, Junior, Larsson EJ, Ching TH. Risk factors for presbycusis in a socio-economic middle-class sample. Braz J Otorhinolaryngol. 2009;75:530–36. doi: 10.1016/S1808-8694(15)30492-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Uchida Y, Nakashimat T, Ando F, et al. Is there a relevant effect of noise and smoking on hearing? A population-based aging study. Int J Audiol. 2005;44:86–91. doi: 10.1080/14992020500031256. [DOI] [PubMed] [Google Scholar]
  • 32.Nomura K, Nakao M, Morimoto T. Effect of smoking on hearing loss: Quality assessment and meta-analysis. Prev Med. 2005;40:138–44. doi: 10.1016/j.ypmed.2004.05.011. [DOI] [PubMed] [Google Scholar]
  • 33.Korres S, Riga M, Balatsouras D, et al. Influence of smoking on developing cochlea. Does smoking during pregnancy affect the amplitudes of transient evoked otoacoustic emissions in newborns? Int J Pediatr Otorhinolaryngol. 2007;71:781–86. doi: 10.1016/j.ijporl.2007.01.015. [DOI] [PubMed] [Google Scholar]
  • 34.Vinay Effect of smoking on transient evoked otoacoustic emissions and contralateral suppression. Auris Nasus Larynx. 2010;37:299–302. doi: 10.1016/j.anl.2009.09.013. [DOI] [PubMed] [Google Scholar]
  • 35.Torre P, Dreisbach LE, Kopke R, et al. Risk factors for distortion product otoacoustic emissions in young men with normal hearing. J Am Acad Audiol. 2007;18:749–59. doi: 10.3766/jaaa.18.9.4. [DOI] [PubMed] [Google Scholar]
  • 36.Cassidy JW, Ditty KM. Gender differences among newborns on a transient otoacoustic emissions test for hearing. J Music Ther. 2001;38:28–35. doi: 10.1093/jmt/38.1.28. [DOI] [PubMed] [Google Scholar]
  • 37.Aidan D, Lestang P, Avan P, Bonfils P. Characteristics of transient-evoked otoacoustic emissions (TEOES) in neonates. Acta Otolaryngol. 1997;117:25–30. doi: 10.3109/00016489709117986. [DOI] [PubMed] [Google Scholar]
  • 38.Pavlovcinova G, Jakubikova J, Trnovec T, et al. A normative study of otoacoustic emissions, ear asymmetry, and gender effect in healthy schoolchildren in Slovakia. Int J Pediatr Otorhinolaryngol. 2010;74:173–77. doi: 10.1016/j.ijporl.2009.11.002. [DOI] [PubMed] [Google Scholar]
  • 39.Nakamagoe M, Tabuchi K, Nishimura B, Hara A. Effects of neuroactive steroids on cochlear hair cell death induced by gentamicin. Steroids. 2011;76:1443–50. doi: 10.1016/j.steroids.2011.07.014. [DOI] [PubMed] [Google Scholar]
  • 40.Motohashi R, Takumida M, Shimizu A, et al. Effects of age and sex on the expression of estrogen receptor alpha and beta in the mouse inner ear. Acta Otolaryngol. 2010;130:204–14. doi: 10.3109/00016480903016570. [DOI] [PubMed] [Google Scholar]
  • 41.Lariscy JT, Hummer RA, Rath JM, et al. Race/ethnicity, nativity, and tobacco use among US young adults: Results from a nationally representative survey. Nicotine Tob Res. 2013;15:1417–26. doi: 10.1093/ntr/nts344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Nakajima M, al’Absi M, Dokam A, et al. Gender differences in patterns and correlates of khat and tobacco use. Nicotine Tab Res. 2013;15:1130–35. doi: 10.1093/ntr/nts257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Roberts B, Gilmore A, Stickley A, et al. Prevalence and psychosocial determinants of nicotine dependence in nine countries of the former Soviet Union. Nicotine Tab Res. 2013;15:271–76. doi: 10.1093/ntr/nts100. [DOI] [PubMed] [Google Scholar]
  • 44.Marlenga B, Berg RL, Linneman JG, et al. Determinants of early-stage hearing loss among a cohort of young workers with 16-year follow-up. Occup Environ Med. 2012;69:479–84. doi: 10.1136/oemed-2011-100464. [DOI] [PubMed] [Google Scholar]

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