Miami University, Oxford, OH
Northwestern University, Evanston, IL
Contact author: Kathleen M. Hutchinson, Department of Speech Pathology and Audiology, Miami University, 2 Bachelor Hall, Oxford, OH 45056. E-mail: hutchik{at}muohio.edu.
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Method: In this cross-sectional study, cardiovascular (CV) health, pure-tone thresholds at 1000 to 4000 Hz, and distortion product otoacoustic emissions (DPOAEs), with and without contralateral noise, were measured in 101 participants age 10–78 years.
Results: Persons in the "old" age category (49–78 years) had worse pure-tone hearing sensitivity and DPOAEs than persons in the younger age categories (p < .05), affirming an age effect. Although hearing decline occurred in all persons in all CV fitness categories of every age group, those with low CV fitness in the old age group had significantly worse pure-tone hearing at 2000 and 4000 Hz (p <.05). Otoacoustic emission measurements were better for the old high-fit group but not significantly influenced by CV fitness level across age groups.
Conclusions: Results of the current study elucidate the potentially positive impact of CV health on hearing sensitivity over time. This finding was particularly robust among older adults.
Key Words: distortion product otoacoustic emissions, suppression, cardiovascular fitness, pure-tone thresholds
A decline in hearing sensitivity is considered a likely consequence of age (Gates & Cooper, 1991; Hull, 1989). However, some initial signs of auditory aging start long before senescence. Early evidence of nerve degeneration in the cochlea secondary to hair cell degeneration was reported by early adolescence nearly 40 years ago (Johnsson & Hawkins, 1972). Numerous studies have reported deterioration of hearing levels at 45–50 years of age and then a notable acceleration above 70 years (Gates & Cooper, 1991; Robinson & Sutton, 1978; Ross, Fujioka, Tremblay, & Picton, 2007; Shuknecht, 1955, 1964, 1974). However, aging is only one of many factors that contribute to a decline in hearing sensitivity. Hearing ability is also commonly compromised by otologic and cardiovascular (CV) disease and exposure to noise.
Previous studies have provided evidence that CV fitness has a protective role in hearing preservation (Alessio, Hutchinson, Price, Reinart, & Sautman, 2002; Cristell, Hutchinson, & Alessio, 1998; Hutchinson et al., 2000; Ismail et al., 1973; Kolkhorst et al., 1998; Manson, Alessio, Cristell, & Hutchinson, 1994). CV fitness was the main health component associated with hearing, with peak oxygen consumption (VO2 peak) as the basis for comparison. Other health and fitness determinants—body composition, blood pressure, and blood lipids—displayed no significant relation to hearing sensitivity (Hutchinson et al., 2000; Kolkhorst et al., 1998), whereas muscle strength was inversely related to hearing sensitivity (Hutchinson et al., 2000). Research in cellular mechanisms in the cochlea revealed that cells under stress from noise, ototoxic drugs, and aging generate proteins to protect surviving cells. Several laboratories have demonstrated positive protective pharmacological effects of specific proteins against cochlear damage (Henderson, Bielefeld, Harris, & Hu, 2006). Antioxidant research has allowed researchers to better understand the effects of certain nutrients on cochlear microcirculation. The results of one randomized controlled trial demonstrated that participants who supplemented their diet with folic acid (an antioxidant that scavenges free radical molecules) for 3 years evidenced improvement in low-frequency behavioral thresholds (Durga, Verhoef, Anteunis, Schouten, & Kok, 2007).
A common explanation of how CV fitness may influence hearing sensitivity is through the effect on blood circulation, especially to the organs and muscles of the inner ear, in particular, the stria vascularis in the cochlea. Metabolism and blood flow are directly related to the vascular pattern of the cochlea. Reduction in blood circulation through the inner ear can also cause reduced hearing sensitivity over time. Variations in cochlear blood flow may affect the availability of oxygen and glucose, which is more rapidly metabolized during sound stimulation (Brant et al., 1996). This hypothesis is difficult to assess in vivo; therefore, knowledge about these interactions is based on descriptive and animal studies. Any decrease in blood flow causes a disruption of the physical and chemical processes by which metabolic energy is created in the cochlea (Cruickshanks et al., 1998).
There is evidence that regular exercise may play a role in hearing conservation via improvements in circulation and VO2 peak. Ismail et al. (1973) had participants complete a 20-week-long physical fitness program, which improved their CV fitness as measured by VO2 peak, as well as their baseline pure-tone thresholds (PTTs). A more recent investigation revealed improved pure-tone and temporary threshold shifts in healthy, young adults with low-average fitness levels who improved their VO2 peak following 8 weeks of twice-weekly aerobic exercise (Cristell et al., 1998). Hutchinson et al. (2000) and Alessio et al. (2002) found PTTs to be specifically related to CV fitness, the premise being that high CV fitness levels are associated with enhanced circulation within the vascular system. Nevertheless, two studies found no consistent pattern between fitness level, exercise, and evoked otoacoustic emission (OAE) amplitudes (Alessio et al., 2002; Engdhal, 1996).
A growing body of evidence has demonstrated the value of evoked OAEs in addition to standard PTTs in revealing the acute effects of noise and ototoxic agents (Engdhal & Kemp, 1996; Ress et al., 1999). OAE testing has been shown to reflect alterations in the cochlea and outer hair cells before a significant hearing loss is present (Arnold, Lonsbury-Martin, & Martin, 1999; Lonsbury-Martin & Martin, 1990; Marshall & Lapsley Miller, 2007; Negley, Katbamna, Crumpton, & Lawson, 2007). OAEs are useful experimentally for evaluating the status of cochlear function in experimental models. They have proven valuable in monitoring the effects of ototoxins and noise on cochlear function. Furthermore, OAEs also provide a means to assess the efferent system.
Though a number of studies have investigated the interconnection between CV health and hearing sensitivity (Alessio et al., 2002; Hutchinson et al., 2000), there is no consensus on the topic. This evidence to date prompts us to examine more closely the relationship of CV fitness level and hearing. The present study evaluated both pure-tone levels and distortion product otoacoustic emission (DPOAE) measures in a representative sample of more than 100 participants categorized by age and fitness abilities. In this cross-sectional study, data were gathered from participants who had been screened for otologic disorders and evidence of noise-induced hearing loss prior to assessment, thus reducing bias due to underlying hearing disorders. It is hypothesized that a healthy CV system attenuates the effects of age on hearing processes, thus maintaining hearing sensitivity and cochlear function.
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Table 1 Sex and age with standard deviations.
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Table 2 Mean pure-tone thresholds by frequency and age groups with standard deviations.
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Annual calibration of audiometric equipment was performed according to ANSI (2004) guidelines. A listening check was performed daily on audiometric equipment.
DPOAEs were recorded using an Otometrics Madsen Capella 503 Cochlear Emissions Analyzer coupled to an IBM personal computer with RS232 cables to present the primary tones and record DPOAEs. Participants were seated quietly and instructed to keep movement to a minimum. The DPOAEs were recorded with the input/output (I/O) function at an audiometric frequency of 4000 Hz by inserting an adult ear probe into the test ear of each participant. Good reliability has been found for DPOAE measurement at 4000 Hz; DPOAEs in the midfrequency range are sensitive to changes caused by aging and noise factors. The I/O function of the 2f1-f2 DPOAE (f1 = 3649 Hz) was recorded. Briefly, I/O curves were obtained at 4000 Hz using equilevel stimuli between 70 and 55 dB SPL in 5-dB increment steps. Because the growth of the distortion product (DP) varies by primary tone level differences (Kummer, Janssen, & Arnold, 1998), the growth of the DPs was measured at equal levels. A limitation of this DPOAE instrument is its inability to vary tone levels continuously instead of in discrete steps. A measurement was considered valid if the signal-to-noise ratio was +3 dB SPL or better (Cilento, Norton, & Gates, 2003). Response amplitude at the four intensity levels was assessed both with and without contralateral white noise.
To assess efferent suppression, the DPOAE was recorded in both the presence and absence of contralateral suppression supplied by white noise (bandwidth of 1600 to 8000 Hz) presented continuously at 84.1 dB SPL by a Beltone 2000 audiometer using an insert earphone in the opposite meatus. Prior to stimulation, the "check probe fit" procedure was performed to ensure accurate fit of the DPOAE probe as well.
The amplitude of the DPOAE responses in relation to the noise floor was noted for each of the eight test conditions; those with a +3-dB SPL signal-to-noise ratio were accepted as valid DPOAEs. The proportions of valid DPOAEs at 55 dB SPL without and with contralateral noise were .96 and .95, respectively; the proportions of valid DPOAEs at 70 dB SPL in the same two conditions were .97 and .98, respectively. The DPOAE data collected at 60 and 65 dB SPL were not included in this report because they paralleled the findings at 55 and 70 dB SPL; additional analyses of repeated measures at all SPLs might reduce the power to detect differences without additional contribution to the experimental questions.
VO2 peak was determined using either a maximal or a submaximal graded exercise test protocol on a Monark Bicycle ergometer. Participants began by pedaling at 50 revolutions/min against a 1-kg resistance for 2 min. Thereafter, resistance was increased 0.5 kg every 2 min. Heart rate response, blood pressure, and respiratory gases were monitored continuously throughout the test. Oxygen uptake was measured by the open-circuit method using a low-resistance, two-way breathing valve. Respiratory gases were analyzed for CO2 and O2 concentrations on Ametek gas analyzers. Modified regulations that required a physician to be present when administering maximum graded exercise tests to participants age 35 years and older forced a switch to use of submaximal exercise tests for most of the participants in this study (American College of Sports Medicine, 2000). The VO2 peak was calculated using a standard Young Men's Christian Association (YMCA) submaximal graded exercise test (Sanders & Duncan, 2006). No test had to be terminated due to participant report of angina or any other abnormal exercise response.
Statistical Analyses
Analyses were done with SPSS Version 16.0. The data were first summarized and examined for outliers and consistency. Multivariate analyses of variance (MANOVAs) were done for four age categories and three fitness levels using PTTs and DPOAE amplitudes as dependent variables. Participants were divided into four age categories containing 22 to 27 participants for analysis purposes: youth = 10 to 19 years; young adult = 20 to 27 years; middle-aged adult = 28 to 48 years; old adult = 49 to 78 years. Dividing participants into four groups for initial analysis enabled large enough samples (n = 22–26) to avoid single participants overwhelming an average across-aged adult responses. The old age participants were lowest in number (n = 22) and spanned the widest age range. The VO2 peak was also analyzed as a categorical variable to represent an individual's CV fitness level (high, medium, or low). In other words, the VO2 peak parameters indicated whether an individual's fitness level acted as a buffer for age-related hearing decrement. Low-fit individuals had an aerobic capacity equal to the least fit 20% of the population for that age group and sex (Sanders & Duncan, 2006). Moderately fit participants had an average aerobic capacity equal to 20%–59% of the population for that age group and sex. The high-fit group had an aerobic capacity equal to the most fit 60%–100% of the population for each age group and sex.
It has been shown that the individuals in the highest fitness level should show less of an age-related impact on pure-tone and DPOAE amplitude test results than those individuals in the lowest fitness level (Alessio et al., 2002). A value of p < .05 was set as the level of statistical significance for all tests reported here. Because significant interactions were present, separate MANOVAs were done for age and fitness variables.
Amplitude measurements obtained at 55 dB and 70 dB SPL and PTTs for the same ear were compared by participants' CV fitness level by age group. Previous research has detailed no effect of sex on DPOAE results (Sheppard, Brown, & Russell, 1996); therefore, no separate sex analyses were done.
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Table 2 illustrates the means of the PTTs by age group; pure-tone levels increased with age, with more variability in the middle and old age groups. Ninety-four percent of the participants had normal PTTs (i.e.,
25 dB HL) at all audiometric frequencies. Examination of Table 2 shows mean thresholds at 1000, 2000, 3000, and 4000 Hz were worse for the middle and old age groups compared with the two younger age categories.
Table 3 shows the mean DPOAE amplitudes both without and with contralateral noise at two intensity levels. The DPOAE amplitudes show a similar pattern to PTTs, with values worsening with increasing age among the middle and old age groups at both intensity levels. Table 3 also illustrates better DPOAE thresholds at 70 dB SPL without noise in comparison to two mean thresholds at 55 dB SPL (with and without contralateral noise).
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Table 3 Mean distortion product otoacoustic emission amplitudes (dB SPL) by intensity and age groups with standard deviations.
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Values of the VO2 peak measurements ranged from 17.2 to 78.6 ml/kg/min, with a mean of 37.6 (SD = 11.4; see Table 4). Because the three fitness categories were determined by participant age and sex, both classification values are listed. Although absolute mean levels appear consistent across age classifications, analysis of variance (ANOVA) follow-up test results show that the values for the youth group classification were significantly better than the old age group, F(3, 100) = 3.78, p <.05.
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Table 4 Mean oxygen consumption values by age group and gender with standard deviations.
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Figure 1 Mean pure-tone (PT) threshold at 1000, 2000, 3000, and 4000 Hz (±SD) by fitness level and age classification. The population was separated into 4 age groups with similar numbers of people in each group.
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The two-factor ANOVA model was repeated to assess the factors of CV fitness and fitness level on DPOAE amplitudes at 4000 Hz at two intensity levels, with and without contralateral noise. Figure 2 illustrates the mean DPOAE thresholds categorized by age and fitness categories. The DPOAE thresholds at 55 dB and 70 dB SPL were significantly better in the youth and young groups in comparison to the two elder age groups, F(3, 100) = 9.26, p < .05. Similarly, the DPOAE level with contralateral noise at 55 dB SPL was also significantly better in the youth group (10–19 years) compared with the middle-age and old age groups, F(3, 100) = 8.11, p < .05. There was no statistical separation of the fitness level factor on DPOAE amplitude in any test condition across age groups (p > .05).
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Figure 2 Mean distortion product otoacoustic emission (DPOAE) thresholds by age and intensity level (±SD).
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Table 5 Slope (β coefficients) and significance (p values) at 55 and 70 dB SPL accounting for pure-tone hearing threshold at 4 kHz.
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Table 5 also displays the slope coefficient (β) for the effect of age and fitness on DPOAE at the two intensity levels when amplitude values were adjusted for hearing threshold level at 4000 Hz; the decline in DPOAE amplitude was attributable to the worsening auditory thresholds. Patterns of DPOAE amplitudes measured with contralateral noise were similar to results found in Table 5. The unique variance of fitness level did not significantly account for DPOAE amplitudes after accounting for the effects of the PTT at 4000 Hz. Multivariate regression findings were consistent with the MANOVA results.
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In our cross-sectional design, mean pure-tone hearing level was most sensitive in the younger age groups. Figure 1 illustrates better hearing levels in the younger groups compared with the old group (age 49–78 years). Hearing levels for the 10–27-year-old participants primarily ranged between –5 and 15 dB HL, whereas the participants age 28 and older ranged between 0 and 40 dB HL across fitness categories. Variability within categories is more evident in the mid- and low-fit levels, showing more dramatic changes between the teen years and early 20s versus middle to old age groups. The PTT range of the high-fit category indicated a narrower range of hearing levels and more consistent, sensitive levels.
Nevertheless, the cross-sectional "snap shots" (see Figure 1) indicate that pure-tone hearing sensitivity is not consistently associated with better CV health at all frequencies. Hearing levels were similar in teens and 20-year-olds within all fitness levels; an increase in pure-tone hearing sensitivity, indicating worse hearing, was observed in the middle and old age range. For the study participants, however, mean PTTs at 2000 and 4000 Hz were significantly better within the high-fit compared with the low-fit old adult group.
Earlier reports have observed significant associations between CV fitness and hearing sensitivity (Alessio & Hutchinson, 1991; Cristell et al., 1998; Hutchinson et al., 2000; Manson et al., 1994). Other laboratories have reported similar results using criteria such as VO2 peak, blood pressure, and percentage body fat to distinguish persons with low and high CV health (Axelsson & Lindgren, 1985; Ismail et al., 1973). Alessio et al. (2002) illustrated better hearing thresholds among high CV health fitness participants compared to the low and medium fitness level groups only at the older ages (i.e., over 55 years). Age 50 appeared to be a separation point, after which fitness level and age were related in a statistically significant direction, with high fitness being positively related to better hearing levels (Alessio et al., 2002). In the current study, primary changes were most prominent for individuals over 60, especially at 4000 Hz or above.
Figure 2 illustrates the decrease of DPOAE amplitude across the age groups by fitness categories. Results show highest amplitudes for all younger participants at both the 55- and 70-dB SPL stimulus levels. CV fitness, as an isolated variable, resulted in stabilization of amplitudes as the participants increased in age over 49 years at both intensity levels. This demonstrated a protective effect of CV fitness on hearing; participant age and 4000-Hz PTT appeared to drive the decrease in levels. Similarly, DPOAE amplitudes with contralateral noise did not exhibit sensitivity to CV health status. In some ears, a small enhancement of DPOAEs created by contralateral stimulation was observed. Similar findings have previously been reported (Grazyna, Smurzynski, Morawski, Namyslowski, & Probst, 2002). With lower and higher levels of fitness, the clinical performance of DPOAEs did not separate groups for early identification for susceptibility to hearing loss. The DPOAE results are consistent with Hutchinson et al.'s (2000) findings; no association was found between fitness and muscle strength measures and DPOAE measures. Cilento et al. (2003) examined the effects of age and PTT shift and also found much variability in DPOAE findings.
Measurement of DPOAEs exhibits properties of suppression, tuning, and vulnerability closely paralleling the properties of hearing. Gains in CV fitness result in changes in underlying physiological mechanisms such as cerebral structure and both cerebral and cochlear blood flow (Colcombe & Kramer, 2003; Torre, Cruickshanks, Klein, Klein, & Nondahl, 2005). CV improvements have led to improved visuospatial and executive control processes. Corticofugal activity has been shown to influence efferent suppression of OAEs (Perrot et al., 2006). Ipsilateral sound stimulation suppresses the contralateral sound-evoked excitation of almost half of inferior colliculus neurons (Faingold, Gehlbach, & Caspary, 1989; Rose, Gross, Geisler, & Hind, 1966). If cortical function is a beneficial consequence of CV fitness training, then subcortical modulation of the evoked OAEs measured from the contralateral ear could also be influenced. The present DPOAE suppression results exhibited much variability and were not sensitive to differences in the function of the efferent system between fitness levels.
Current results support the statistical inferential association between CV fitness and pure-tone hearing ability preservation across a 68-year time period. Moderate and high CV fitness levels have protected against temporary hearing loss caused by noise (Hutchinson et al., 2000; Manson et al., 1994). Current concepts in auditory physiology include an active mechanism that serves to counteract the effects of trauma and stress (Campbell et al., 2003; Henderson, Subramaniam, & Boettcher, 1993; Patuzzi, 1992). The observations that hair cells contain specific proteins that undergo changes in expression with slight edema suggest that active elements exist to protect tissue from damage. Such proteins may also play key roles in protecting the hair cell from metabolic and aging changes, as has been suggested as the function of stress-induced proteins (Campbell et al., 2003; Lindquist, 1986). Other studies have also raised the possibility that stress proteins could protect the auditory periphery from damage due to noise, ototoxic drugs, or trauma (Patuzzi, 1992).
A limitation of this study is that it was a cross-sectional analysis of the relation between fitness and hearing function. Directionality associations cannot be inferred from this investigation, as cochlear and brainstem function preceded fitness level achievement or the measured fitness level preceded auditory function. Another limitation of this study was self-reported history of lifestyle factors (i.e., smoking, noise exposure, medication use, activity, and alcohol). Some participants may have misrepresented their health history during the questionnaire interview. Misinformation may bias the association either in favor or away from the null hypothesis. An evaluation of the pure-tone levels and DPOAE levels of participants in a 5-year follow-up study may help clarify whether cochlear hearing function is influenced by CV health. Despite the adequate sample size, comparison of these results with other CV analyses of age-related hearing loss will be an important next step to confirm the long-term effects of health on cochlear function.
Accumulating evidence has pointed to a large number of physiological, psychological, and sociological risk factors that are either directly or indirectly related to late-onset hearing loss (Gates & Cooper, 1991). Although different mechanisms underlie these various types of stressors, commonalities exist including free radical formation and alterations in the body's antioxidant activity (Wang, Puel, & Bobbin, 2007). The current state of knowledge regarding the interaction of risk factors for hearing loss is still limited. Genetics, nutrition, and pharmacological factors have been shown to play a role in the susceptibility to hearing loss (Campbell & Rybak, 2007; Gates, Schmid, Kujawa, Nam, & D'Agostino, 2000; Wang et al., 2007). It is generally accepted that antioxidative mechanisms in the vasculature protect the auditory system from excessive free radical formation. An imbalance favoring free radicals over antioxidant activity results in oxidative stress and may result in a suppressed ability to repair cellular function (Cruickshanks et al., 1998). Antioxidant levels can be increased from nutritional supplementation as well as with regular exercise. A large number of exercise studies, both acute and chronic (Alessio & Blasi, 1997), indicate a protective role of regular exercise in boosting antioxidants, especially during exertion or stress, when free radicals are elevated. In this way, physical activity positively affects cellular mechanisms related to oxidative stress.
In summary, although hearing sensitivity and age were negatively related, considerable variability existed among hearing levels for the old adult cohorts as well as within the different fitness categories. High CV fitness was associated with the best PTTs in the old adult participants, suggesting that high CV fitness protected and preserved hearing in high-fit persons regardless of other factors. In the teens and 20s, persons with moderate and low CV fitness displayed good hearing between –5 and 15 dB HL, experienced worse hearing as they became older, and demonstrated high variability in hearing threshold levels. The DPOAE thresholds appeared at higher amplitudes among the younger participants and stabilized among the most fit participants as they aged.
Most certainly, the dedicated and steady accumulation of scientific knowledge about the processes that protect hearing decrement lay the basis for developing successful clinical applications for incorporation of remediation approaches. The ways regular physical activity affect health and longevity have, in the past, focused on improved CV health and cancer prevention. Another explanation is that physically active individuals may be better equipped to handle acute oxidative stress associated with disease or other metabolic stressors (Colcombe & Kramer, 2003). While a general measure of physical fitness using maximum oxygen consumption may be less sensitive to subclinical circulation patterns, the current study points to the beneficial influence of CV health on hearing function, especially as one ages.
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Received April 9, 2009
Revision received July 3, 2009
Accepted December 21, 2009
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