Introduction
Although the link between cigarette smoking and peripheral hearing loss was established over 40 years ago, information on the effects of smoking at the cochlear and auditory central nervous system levels has become available only recently. Work on otoacoustic emissions and several tests designed to tap into structural and functional aspects of the auditory central nervous system indicate that not only are the outer hair cells of the cochlea susceptible to damage, but that smoking may affect many aspects of central auditory processing. Furthermore, adolescents and children of mothers who smoked during pregnancy are particularly vulnerable to the effects of cigarette smoking. This review describes the effects of smoking on the peripheral and central auditory nervous system and presents tentative hypotheses regarding mechanisms of damage.
Prevalence
The most recent health risk behavior survey conducted by the Center for Disease Control and Prevention (CDC, 2007; 2008) indicates that approximately 10% of students in grades 9 through 12 currently smoke more than 10 cigarettes per day. In the 18-64 year age range the prevalence increases to approximately 20%, with a slightly lower prevalence rate in females than in males across the age span (CDC, 2007; 2008). Moreover, estimates of women who smoke during pregnancy indicate an overall prevalence of 11.4%, with a range of 6.3% to as high as 26.2% when state-specific data are evaluated (CDC, 2004).
Although hearing impairment statistics in newborns, children, and adolescents associated with prenatal and/or postnatal exposure to cigarette smoking is not available, several epidemiological studies over the years have indicated an increase in the prevalence of hearing loss as a function of age. For example, Cruickshanks, Klein, Klein, Wiley, Nondahl, and Tweed (1998) showed that the prevalence of hearing loss (pure-tone average in the 0.5-4 kHz range of> 25 dB in the worse ear) in current smokers increased from 26% in the 48-59 years age range to 56% and 71% in the sixth and seventh decades of life, respectively. Furthermore, as pack years of cigarette smoking (number of cigarettes smoked per day divided by the number of years of smoking) increased from 0 to> 40, the prevalence of hearing loss increased from 17% to 29% in the 48-59 years age range, from 36% to 59% in the 60-69 year old smokers, and from 60% to 74% in the 70-79 year old smokers. In younger subjects, Sharabi, Reshef-Haran, Burstein, and Eldad (2002) showed that 20-35 year-old smokers were at a greater risk for hearing impairment (43%) as compared to those over 35 years of age (17%). These prevalence numbers indicate that not only does cigarette smoking place an individual at risk for hearing loss, but that as pack years of smoking increase accompanying hearing loss also increases and that the effects of smoking may be exacerbated in younger individuals.
Influence of smoking on peripheral hearing
Although deleterious effects of cigarette smoking on adult health have been well documented, only recently have clinical studies linked adverse neurodevelopmental problems to prenatal exposure associated with maternal smoking. Thus, this overview will address the effects of cigarette smoking on the auditory system from both perspectives: the effects of smoking in adults and the effects associated with maternal smoking.
Conductive vs. sensorineural hearing loss
Cigarette smokers are exposed to nicotine directly, as well as a number of additional chemicals including formaldehyde, benzene, arsenic, vinyl chloride, ammonia and hydrogen cyanide via secondhand smoke inhalation (CDC, 2006). Studies have correlated the presence of cotinine, a chemical that has been identified as a biomarker of secondhand smoke exposure, with upper respiratory tract problems and increased risk for middle ear problems (CDC, 2006). The study by Sharabi et al. (2002) showed that conductive hearing loss was most prevalent in all subject groups (age range 20-68 years). Overall, 6.1% of current and past smokers experienced conductive hearing loss of at least a mild degree (> 30 dB across the 0.25-8 kHz range). Smokers were also twice more likely to experience a mild sensorineural hearing loss (> 25 dB either in the low or high frequencies) compared to nonsmokers. Nakanishi, Okamoto, Nakamura, Suzuki, and Tatara (2000) showed that male office workers in the 30-59 year age range who smoked were at a greater risk for hearing loss at 4 kHz than at 1 kHz compared to nonsmokers and ex-smokers. In their study, they controlled for age and a number of health factors like body mass index, alcohol consumption, triglyceride levels, etc., and showed that as numbers of cigarettes smoked per day and pack years of smoking increased, the risk for high-frequency hearing loss increased in a dose dependent manner, whereas low-frequency hearing loss remained unchanged.
Smoking and ultra high-frequency hearing
There is limited data on ultra high-frequency (9-20 kHz) changes associated with cigarette smoking. A study by Cunningham and colleagues (1983) showed a trend towards increased hearing thresholds in the ultra high-frequency range in 20-35 year-old current cigarette smokers as compared to nonsmokers. However, there was considerable variability in the data so that the results were statistically significant only at 9 kHz. The data from our laboratory (Negley, Katbamna, Crumpton, and Lawson, 2007), likewise, showed no differences in ultra high-frequency hearing of smokers and nonsmokers in the 20-30 year age range.
Combined effects of smoking, noise exposure and aging on hearing
A number of studies have shown that noise induced hearing loss is exacerbated by cigarette smoking and that the effects of age may further compound the hearing problem. Most recently, Wild and colleagues (2005) noted that long-term cigarette smokers with occupational noise exposure may be at a greater risk for developing a permanent hearing loss at high frequencies (3-4 kHz) than nonsmokers with a similar history of occupational noise exposure. Likewise, Mizoue, Miyamoto, and Shimuza (2003) showed that the effects of smoking and noise exposure were additive, so that high-frequency hearing loss in smokers may be added to noise exposure effects.
Noorhassim and Rampal (1998) investigated the combined effects of smoking and age on hearing and showed that pack years of smoking and age served as significant risk factors for hearing impairment. The prevalence rates of hearing loss in smokers 40 years of age. Although nonsmokers also showed some increase in hearing loss as a function of age, the effect was not pronounced. Based on further calculations, they indicated that the effects of smoking and aging were multiplicative, thereby explaining the remarkable augmentation of hearing loss noted in their work.
In their assessment of the effects of age, noise-induced hearing loss, and confounders, Toppila, Pyykko, and Starck (2001) showed that confounders like smoking, serum cholesterol, systolic or diastolic blood pressure and use of analgesics greatly influenced the hearing status of young and elderly subjects. However, even when subjects were matched in pairs by age, noise exposure, blood pressure and serum cholesterol, older subjects tended to be more susceptible to noise-induced hearing loss than younger subjects, indicating that age in itself may be a determinant of susceptibility to hearing loss.
Ferrite and Santana (2005) showed that smoking, age, and noise exposure together pose a greater risk for hearing loss than each factor alone. They showed that non-exposed nonsmokers in the 20-40 years age category were least likely to experience hearing loss, whereas smokers over 40 years with a history of noise exposure were most likely to show a hearing loss. They suggested that these synergistic effects were most consistent with biological interactions.
All of the above studies indicate that although age in itself may produce a decline in hearing over time, the contributions of a variety of risk factors including smoking further perpetuate the hearing loss. Thus, if individuals monitor risk factors like blood pressure, diabetes, cholesterol, body mass index, etc., and choose a healthy lifestyle that promotes good cardiovascular health, age related hearing loss may be abated considerably. In fact, a recent survey of 4,083 individuals in the 53-67 years age range supports such a positive outcome, indicating that reduction of medical and environmental risk factors (including smoking) may be effective hearing conservation strategies, in addition to promoting overall good health as a function of age (Fransen et al., 2008).
Smoking and otoacoustic emissions
There are only two studies in literature that describe the effects of cigarette smoking on otoacoustic emissions (OAEs). A study conducted in our laboratory (Negley et al., 2007) examined distortion product OAEs (DPOAEs) in 20-30 year old smokers who smoked for 5-8 years and who reported essentially no history of noise exposure. All subjects were screened with tympanometry to rule out middle ear problems bilaterally. Results of pure-tone audiometry showed normal hearing sensitivity in the conventional frequency range, although there was a trend of increased thresholds (2-10 dB) across all frequencies with a significant elevation of 10 dB at 6 kHz in smokers compared to nonsmokers. As stated above, ultra high-frequency hearing was age appropriate, with no significant differences across smoker and nonsmoker groups. DPOAEs measured at both high (L1=L2=70 dB SPL) and moderate (L1=65 dB SPL and L2=50 dB SPL) intensity levels showed reduced emission amplitudes in the 2-8 kHz range in smokers, but no differences in the noise floors across the frequency range when compared to nonsmokers. Mean input/output (I/O) detection thresholds measured at f2 frequencies of 2, 4 and 8 kHz were also significantly elevated in smokers compared to nonsmokers. Since the metabolic status of the cochlea influences DPOAE growth function curves, increased thresholds provide a critical gauge of the cochlear metabolic dysfunction. There is now evidence that the cochlear stria vascularis may undergo age related changes in the absence of any outer hair cell damage and that such changes in the cochlear status may be picked up in the I/O response curves (e.g., Schmiedt, Lang, Okamura, & Schulte, 2002). Thus, DPOAE I/O threshold elevations in smokers may be a reflection of metabolic changes in the cochlear amplifier.
Another study measured transiently evoked OAEs (TEOAEs) in newborns with a maternal history of cigarette smoking during pregnancy (Korres et al., 2007). Recordings were obtained 24-48 hours after birth from 50 males and 50 females who experienced prenatal exposure to cigarette smoking and were compared to an age- and gender-matched control group of babies without a history of maternal smoking. The babies were further subdivided into low, moderate and high exposure groups based on the number of cigarettes smoked by the mother (low=less than 5 cigarettes/day; moderate=5-10 cigarettes/day; high=more than 10 cigarettes/day). Results showed a significant decline in the mean TEOAE response amplitude in babies exposed to high levels of smoking compared to the control group of babies, plus a significant reduction in TEOAE amplitude at 4 kHz in all exposure groups compared to the control group. Thus, cigarette smoking is detrimental to the developing cochlea, and the effects of cigarette exposure are already apparent and assessable at birth.
Central auditory nervous system deficits associated with cigarette smoking
Auditory cognitive processing difficulties in adult smokers
Although a few studies have examined the effects of cigarette smoking on auditory attention, arousal and cognitive processing, the outcomes have been inconsistent. For example, Kishimoto and Domino (1998) measured auditory middle latency responses (AMLR) in smokers both after a smoking session and after overnight abstinence from smoking and then compared the results to those obtained from nonsmokers. The outcomes showed significantly reduced Na and Pa component latencies during smoking, as compared to AMLR measurements during abstinence and the results from nonsmokers. Likewise, component amplitudes of auditory brainstem response wave V-Na, Na-Pa and Pa-Nb were significantly enlarged during smoking, as opposed to the results obtained during abstinence and those obtained from nonsmokers. Since AMLR originates from auditory thalamocortical pathways with some contributions from the inferior colliculus and reticular formation, the AMLR findings in smokers were attributed to changes in arousal and information processing. The authors concluded that cigarette smoking appears to increase the arousal state and to enhance sensory information processing.
A more recent study that used auditory cortical evoked potentials as a measure of cognitive processing, however, showed no differences in measurement outcomes recorded from smokers as compared to nonsmokers (Ascioglu, Dolu, Golgeli, Suer, & Ozesmi, 2004). These investigators used stringent subject selection criteria; smokers and nonsmokers were 23 (+2.3) year-old medical students and the smokers used an average of 14 (+4.2) cigarettes/day for more than one year. A standard oddball paradigm was used to evoke auditory late (ALR) and P300 responses. Recordings were obtained from Fz, Cz and Pz electrode sites, and ALR components N1, P2, N2 and P300 responses were measured. The results showed no significant differences in any component latencies or amplitudes of ALR or P300 responses obtained from smokers and nonsmokers.
Contrary to the above findings, another study including subjects with chronic nicotine use measuring P300 using a similar oddball paradigm and electrode recording sites showed a significant reduction in P300 amplitudes, but no latency changes in nicotine users as compared to control subjects (Muller et al., 2007). These findings suggest that chronic nicotine use impairs cognitive auditory processing. Such discrepancies in literature may be attributed to not only variations in pack years and numbers of cigarette smoking, but also to confounding environmental influences.
Auditory/speech processing difficulties associated with prenatal exposure to cigarette smoke
Most of the work linking neurodevelopmental problems in children to cigarette smoking has been conducted on offspring exposed to maternal cigarette smoking. Such an approach not only helps identify neurocognitive impairment during early life and provide early intervention, but also helps to control or restrict the effects of environmental influences. A recent study that measured high-density event related potentials (ERPs) within 48 hours of birth in healthy babies of smoking and nonsmoking mothers showed significant differences in auditory neurophysiology of exposed and non-exposed babies (Key et al., 2007). ERPs are time-locked changes to stimulus onset in an ongoing electroencephalogram (EEG); the stimuli in this experiment were 6 randomly presented consonant-vowel syllables. While the ERPs of non-exposed babies showed hemispheric asymmetries with a larger ERP amplitude over the left than the right hemisphere, especially over the temporal regions, exposed babies either showed no hemispheric differences or showed inconsistencies, with larger amplitudes over the left hemisphere for some, but not all, speech sounds. Furthermore, in the exposed-baby group the ERPs were delayed by 150 ms and they discriminated fewer consonant-vowel combinations than the non-exposed babies. These findings indicate that prenatal cigarette smoke exposure alters speech sound or auditory discrimination ability, and that such changes may ultimately be responsible for not only developmental speech-language problems, but also neurocognitive impairments documented at later ages.
The notion that auditory processing is vulnerable to prenatal smoke exposure is further endorsed by findings that have shown poor performance on a variety of tasks requiring auditory comprehension and processing. Some examples include auditory vigilance, auditory components of speech-language assessment tools and central auditory processing tests (Kristjansson, Fried, & Watkinson, 1989; Makin, Fried, & Watkinson, 1991; McCartney, Fried, & Watkinson, 1994). McCartney and colleagues (1994) showed that 6-11 year old children who were exposed to maternal smoking performed poorly overall on the screening auditory processing test (SCAN), but particularly on the competing word subtest. Even when the data were adjusted for other environmental variables like drug use, demographic variables and passive smoke exposure, the findings did not change. Moreover, children of nonsmokers who were exposed to secondhand smoke showed results that were identical to those children who were exposed prenatally. These findings clearly indicate that auditory maturation is ongoing through at least these ages (6-11 years) and that secondhand smoke may place a child at risk for cognitive impairments.
Results of recent work on adolescent exposure to cigarette smoke reinforces this idea that the adolescent auditory nervous system is still undergoing maturational changes and is vulnerable to damage from cigarette smoking initiated during adolescence (Jacobsen, Slotkin, Menci, Frost, & Pugh, 2007a; Jacobsen et al., 2007b). Moreover, neurocognitive impairments associated with adolescent smoking are no different from those observed in adolescents with prenatal exposure. These studies examined functional and anatomical magnetic resonance images and diffusion tensor images (a technique that measures diffusion of water through brain tissue), to assay functional and structural changes in specific regions of the brain, which in turn may be correlated with developmental changes in cognitive abilities. The tasks utilized during these imaging techniques were primarily auditory and visual attention tasks. The results showed gender-specific adverse effects on both auditory and visual tasks. Whereas females with combined (prenatal and adolescent) exposure to smoke showed greater impairments in auditory and visual attention than either exposure alone, male subjects with combined exposure showed greater impairments in auditory attention alone (Jacobsen et al., 2007a). Results of diffusion tensor imaging showed that auditory thalamocortical and corticofugal pathways are particularly vulnerable to the effects of nicotine exposure, reducing the efficiency of these auditory circuits in auditory processing (Jacobsen et al., 2007b).
An examination of speech-language abilities of children through early teen years further corroborates the impressions of auditory processing impairments related to prenatal smoke exposure. Obel, Henrikson, Hedegaard, Secher, and Ostergaard, (1998) noted that maternal use of more than 10 cigarettes per day during pregnancy produced significant reduction in babbling in babies and that the risk of not babbling doubled by 8 months of age. This risk further increased in children who were breast fed for less than 4 months (Obel et al., 1998). At 12 and 24 months of age, slower auditory habitutation, increased hearing thresholds and decreased scores on tests that require auditory processing were still apparent in children born to smoking mothers (Fried and Watkinson, 1988). These same children continued to score much lower on standardized tests of language development at 3 and 4 years of age, with effects persisting through at least 12 years of age (Fergusson, Horwood, & Lynskey, 1993; Fried and Watkinson, 1988; 2000; Fried, Watkinson, & Siegel, 1997; Fried, Watkinson, & Gray 1998).
The implication of all these outcomes is that extensive maturational changes in auditory neural circuitry continues through adolescence and that smoking during this developmentally sensitive period places the auditory nervous system at risk for permanent damage. These results also indicate that comprehensive audiological evaluations should include tests of auditory processing abilities, in addition to pure-tone and speech audiometry and OAE tests. Explicit information on changes at the peripheral and central auditory nervous system levels may ultimately help dissuade not only pregnant women, but also adolescents and young adults from smoking or abandoning it entirely. The information may also help with therapeutic planning and early auditory and speech-language intervention in children.
Mechanisms of damage associated with cigarette smoking
There is no direct evidence for the mechanisms of damage to the auditory system associated with cigarette smoke exposure. However, at least three different putative mechanisms may play a role in the manifestations of peripheral and central auditory problems associated with nicotine exposure. The first mechanism may be related to hypoxia; both nicotine and carbon monoxide in cigarette smoke have been shown to reduce the oxygen supply to fetal tissue by restricting utero-placental blood flow (Morrow, Ritchie, & Bull, 1988; Albuquerque, Smith, Johnson, Chao, & Harding, 2004). Moreover, there may be direct intake of nicotine by the fetus, since nicotine can easily cross the placenta, potentially increasing fetal nicotine plasma levels by up to 15% and amniotic fluid levels by up to 54% in the mid trimester (Lambers and Clark, 1996). Thus, nicotine-induced vasospasms and carbon monoxide may deplete oxygen levels to the cochlea (Morrow et al., 1988; Albuquerque et al., 2004), thereby explaining OAE amplitude reductions in prenatally exposed babies (Korres et al., 2007). In older individuals nicotine induced vasospasms as well as atherosclerotic damage may play a role in perpetrating (hypoxic) damage to the cochlea and even spiral ganglion cells (Howard et al., 1998).
The second putative mechanism may pertain to the interaction between nicotine and nicotinic acetylcholine receptors (nAChRs) within the auditory system. Nicotine binds to nAChRs that normally modulate the effects of a neurotransmitter called acetylcholine. Since neurotransmitters function as chemical message carriers facilitating communication between cells by binding to the receptors on the cell surface, loss or damage of the receptors in essence would eliminate the modulatory influences of the receptors. There is now evidence that nAChRs are critical components of the auditory pathway, from the cochlea to the temporal lobe, and the descending auditory pathway (e.g., Morley, 2005; Lustig, 2006). Moreover, emerging data indicates that prenatal exposure to nicotine or chronic nicotine use during adolescence damages the nAChR binding sites, producing cognitive impairments in the auditory and visual modalities (Liang et al., 2006; Jacobsen et al., 2007a; 2007b).
Finally, the neurophysiological mechanism that may potentially explain the association between adolescent smoking and neurocognitive deficits is protracted development of the auditory central nervous system pathways. There is incontrovertible evidence that many components of auditory central nervous system development, including the auditory thalamocortical and cortigofugal pathways, continue into late adolescence (e.g., Paus et al., 1999; Jacobsen et al., 2007a; 2007b). Moreover, these pathways are particularly susceptible to damage, if environmental toxins like nicotine are introduced during their developmental emergence (Rice and Barone, 2000; Liang et al. 2006).
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Howard, G., Wagenknecht, L., Burke, G., Diez-Roux, A., Evans, G., McGovern, P., Nieto, J., & Tell, G. (1998). Cigarette smoking and progression of atherosclerosis: The atherosclerosis risk in communities study. Journal of the American Medical Association, 279, 119-124.
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References
Albuquerque, C. A., Smith, K. R., Johnson, C., Chao, R., & Harding, R. (2004). Influence of maternal tobacco smoking during pregnancy on uterine, umbilical and fetal cerebral artery blood flows. Early Human Development, 80, 31-42.
Ascioglu, M., Dolu, N., Golgeli, A., Suer, C., & Ozesmi, C. (2004). Effects of cigarette smoking on cognitive processing. International Journal of Neuroscience, 114, 381-390.
Centers for Disease Control and Prevention. (2004). Smoking during pregnancy - United States, 1990-2002. Morbidity Mortality Weekly Report, 53(39), 911-915.
Centers for Disease Control and Prevention. (2006). The health consequences of involuntary exposure to tobacco smoke: A report of the surgeon general. US Department of Health and Human Services. Retrieved August 19, 2008, from www.surgeongeneral.gov/library
Centers for Disease Control and Prevention. (2007). Cigarette smoking among adults-United States, 2006. Morbidity Mortality Weekly Report, 56(44), 1157-1161.
Centers for Disease Control and Prevention. (2008). Youth risk behavior surveillance-United States, 2007. Surveillance summaries, June 6, 2008. Morbidity Mortality Weekly Report, 57(SS4), 1-136.
Cruickshanks, K., Klein, R., Klein, B., Wiley, T., Nondahl, D., & Tweed, T. (1998). Cigarette smoking and hearing loss: the epidemiology of hearing loss study. Journal of the American Medical Association, 279, 1715-1719.
Fergusson, D. M., Horwood, L. J., & Lynskey, M. T. (1993). Maternal smoking before and after pregnancy: effects on behavioral outcomes in middle childhood. Pediatrics, 92, 815-822.
Ferrite, S., Santana, V. (2005). Joint effect of smoking, noise exposure and age on hearing loss. Occupational Medicine, 55, 48-53.
Fransen, E., Topsakal, V., Hendrickx, J-J., Laer L. V., Huyghe, J. R., et al. (2008). Occupational noise, smoking, and a high body mass index are risk factors for age-related hearing impairment and moderate alcohol consumption is protective: A European population-based multicenter study. Journal of the Association for Research in Otolaryngology, 9, 264-276.
Fried, P. A., & Watkinson, B. (1988). 12 and 24 month neurobehavioral follow-up of children prenatally exposed to marihuana, cigarettes and alcohol. Neurotoxicology and Teratology, 10, 305-313.
Fried, P. A., Watkinson, B., & Siegel, L.S. (1997). Reading and language in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicology and Teratology, 19, 171-183.
Fried, P. A., Watkinson, B., & Gray, R. (1998). Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicology and Teratology, 20, 293-306.
Fried, P. A., & Watkinson, B. (2000). Visuoperceptual functioning differences in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicology and Teratology, 22, 11-20.
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