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Impact of Aging on the Voice

Abdul-Latif Hamdan, Robert Thayer Sataloff, and Mary J. Hawkshaw

Aging is inevitable. It is the end result of cumulative physiologic and pathologic events that lead to senility of structures within our body. It is a natural process that affects all systems leading to laxity, decrease in strength, instability, and weakness. Plato described the elderly Cepahlus in the opening of the Republic as physically withdrawn with reduction in his physical strength.¹ In his theory on gerotranscendence, the inner awakening for metaphysical contemplation in the elderly is triggered by the decline in physical function and its subsequent morphologic changes.

The function of the phonatory system, like any other system in the body, is affected by aging. The senile changes in the larynx result in an increase in its non-linear behavior, thus leading to changes in voice quality classified as presbysphonia.² This condition is on the rise nowadays with the increase in the aging population. It is estimated to reach up to 30% based on numerous epidemiologic reports, with a chronicity rate of 60%.^3–5 Social and behavioral factors may contribute to its high prevalence. In a large cross-sectional study looking at prevalence of dysphonia in elderly subjects, the odds ratio for urban residence and poor social status were reported to be 1.83 and 2.99, respectively.⁶

Dysphonia in the Elderly

Dysphonia is common in the elderly. Based on an epidemiologic study by Roy et al, the life prevalence of dysphonia has been estimated to be 47%.³ However, it is important to note that age-related change in voice quality is not the only cause of dysphonia in the elderly. The prevalence of presbyphonia is markedly surpassed by other causes of dysphonia.^3,7,8 In an investigation on dysphonia in 151 elderly individuals, Woo et al reported the presence of systemic diseases and the use of chronic medications in 53.6% and 40.3% of the cases, respectively.⁴ Similarly, the study by Gregory et al, on voice disorders in elderly patients, revealed the presence of one or more pathologic factors that contributed to dysphonia in all the subjects investigated. In that study, 91% had laryngopharyngeal reflux disease, 73% had muscle tension dysphonia, and 72% had vocal fold paresis.⁹ In another study by Çiyiltepe and Şenkal conducted on 91 patients, vocal nodules, laryngopharyngeal reflux disease and vocal fold paresis were present in 23.9%, 10.8%, and 9.78% of the cases, respectively.¹⁰ This high prevalence of co-morbidities emphasizes the need for an adequate laryngeal examination and a thorough investigation in an elderly patient presenting with dysphonia. Systemic diseases must be sought diligently even after diagnosing or excluding infectious, benign, and malignant causes of dysphonia as local and systemic disorders co-exists.^4,11,12 To that end, presbyphonia should be diagnosed only after all other diagnoses have been established or excluded.

Presbyphonia

Self-Reported Symptoms, Perceptual Properties, and Acoustic Findings In the Elderly

Patients with presbyphonia typically complain of roughness, change in vocal pitch, vocal instability, and weakness, in addition to inability to project the voice and loss of range. Symptoms such as throat clearing and excessive mucus also are often described.¹³ These self-reported complaints, which may impact the ability to communicate in a noisy environment, also are perceived by trained listeners.^14–18 Perceptual evaluation of the elderly voice often reveals asthenia, breathiness, and/or straining. In a report by Honjo and Isshiki in 1980, the voices of elderly women aged between 69 and 85 years were described perceptually as rough and hoarse in comparison to young women.¹⁹ Acoustic analysis reveals often an increase in perturbation parameters, namely, cycle-to-cycle variation in frequency (jitter) and intensity (shimmer), and an increase in noise-to-harmonic ratio.^20–22 In a report by Linville in 1987 on acoustic changes in elderly women, she reported an increase in frequency variability (standard deviation) with aging.²⁰ Similarly, Ferrand, in his investigation on acoustic measures in vocal aging, highlighted the high sensitivity of noise-to-harmonic ratio as an acoustic cue in comparison to other acoustic measures such as cycle-to-cycle variation in frequency.²¹ In another study, Harnsberger et al reported that vocal tremor, degree of noise, and rate of speech can shift the perception of age by 12 years. The authors reached that conclusion by manipulating the degree of noise and tremor in resynthesized voice samples obtained from 10 young male subjects.²²

The aging voice also is characterized by a change in the mean fundamental frequency (F0) and habitual pitch, with a consensus that there is an increase in men by an average of 35 Hz and a decrease in women by an average of 10 to 15 Hz,^23–25 although these data remain controversial. In the study by Honjo and Isshiki on 40 elderly women and men, the authors reported elevated fundamental frequency in men and reduced fundamental frequency in women.¹⁹ The increase in F0 in men was attributed to atrophic changes in the vocal fold musculature and stiffening of the vocal ligament, whereas the decreased F0 in women was attributed primarily to edematous changes of the vocal folds. Similarly, in another longitudinal study of women using archival data, Russell et al reported significant lowering in speaking fundamental frequency with age. The results were obtained by comparing the recordings of women across a 50-year time span.²⁶ Numerous other studies reported different changes in F0 with aging.^27–29 Endres, Bambach, and Flosser reported a decrease in the mean pitch frequency with aging in a sample of four male voices and two female voices. The authors reported that with age formants moves toward lower frequencies.²⁸ Krook in 1988 reported data on speaking fundamental frequency in a group of 467 females and 198 males of different age groups. The results indicated that the mean SFF in the female group, which averaged 188 Hz, decreased until the age of 70 years but then tended to increase after that age. In men, the mean SFF averaged 116 Hz at a young age and tended to rise after middle age.²⁷ In another study by Benjamin on frequency variability conducted on 20 males and 20 females, the author reported a decrease rather than an increase in modal frequency in elderly men with aging (110.3 Hz vs 103.0 Hz).²⁹ A possible explanation for these conflicting reports is the high within-subject variability in elderly subjects and the possible contributing factor of hormonal changes in women after menopause, the impact of which may mask or heighten other effects of aging on voice.

Variation in speech intensity with aging also has been thoroughly investigated in the literature. Morris and Brown in 1994 investigated the effect of aging on speech intensity in women. The study was performed on two groups of women, young (20–35 years) and elderly (70–90 years), who were asked to read the “Rainbow Passage “and to sustain the vowel / α / at different intensities. The results indicated that elderly women had higher minimum intensity level and lower maximum intensity level during vowel production compared to young women.³⁰ In addition to the changes in speech intensity with age, there are also changes in speech intensity modulation and control of vocal loudness. Elderly patients are described as having either decreased loudness, or increased loudness often attributed to impaired hearing. In the study by Baker et al on control of vocal loudness in adults, the authors reported lower sound pressure levels at three levels of loudness in elderly subjects compared to young subjects.³¹ The similarity in subglottal pressure values and the dissimilarity in laryngeal electromyographic activities between both groups alluded to a laryngeal cause for these differences.³¹ Similarly, an investigation by Hodge et al on vocal intensity in elderly versus a control group showed a significant difference between the two groups.³² Sound pressure level and peak airflow were lower in the elderly compared to controls. However, there were no significant differences in the maximum flow declination, phonatory threshold pressure, or fundamental frequency between the two groups.

In conclusion, it is important to note that high intensity phonation plays an important role in accentuating the presence of phonatory changes, which may not be apparent when habitual intensity level is used.³³

Resonance with Aging

In addition to the aforementioned changes in F0 and perturbation parameters, formants’ position and dispersion also may be affected with aging.²⁸ Acoustic measures extrapolated from sustained vowels and connected speech often reveal a shift of formants towards lower frequencies. A study by Linville and Fisher in 1985 on formant frequencies in a group of 75 women stratified into three age groups, showed a decrease in resonance peaks F1 and F2 with aging.³⁴ The analysis was performed on both sustained spoken and whispered vowels. Similar findings were reported few years later, in another investigation by Scukanec et al.³⁵ The authors reported significant lowering of F1 on four vowels and significant lowering of F2 on vowel / α / and /u/ with aging in women. In another study by Linville and Rens in 2001 measuring the first three spectral peaks during connected speech (reading the first paragraph of the Rainbow Passage), the authors showed clearly significant lowering of the first peak with age in both genders, and significant lowering of the second and third peaks in women. The decline in frequency for peaks 1, 2, and 3 in women compared to men were 29% versus 11%, 10% versus 2%, and 9% versus 2%, respectively. This gender effect on formant lowering with age has been attributed to a higher degree of the vocal tract lengthening in women compared to men.³⁶ The accentuated drop in the suspended position of the larynx secondary to weakening of the strap muscles is further enhanced by the loss of vertebral support in women with osteoporosis.³⁷ A study by Xue and Hao in 2003 on vocal tract changes with aging, revealed lengthening and enlargement of the oral cavity with significant increase in the volume of the vocal tract. Acoustic analysis of formant frequencies in groups of young and elderly men and women showed lowering of formant frequencies F1 for five vowels in men and for 7 vowels in women. Commensurate with these acoustic changes were anatomical differences in oral cavity length and volume, and in vocal tract volume but not length. The authors alluded to the importance of vocal tract volume as a determinant of formant measures in addition to vocal tract length. Two other important findings were the similarity in senile changes in both genders and the differential effect of aging on various segments of the vocal tract. Noteworthy is the enlargement and lengthening of the oral cavity and not the pharyngeal cavity.³⁸ A more recent study by Eichhorn et al on the effects of aging on the first four formants in a group of 43 men and 53 women, revealed a mild change in the formants frequencies of the corner vowels secondary to compensatory behavior.³⁹

Laryngeal Airflow Measurements with Aging

Studies on laryngeal airway resistance and airflow measures in the elderly are conflicting. Hoit and Hixon in their investigation on laryngeal valving economy in a group of 70 women of different age groups (10 at each age of 25, 35, 45, 55, 65, 75, and 85 years) reported no significant difference in laryngeal airway resistance with aging, although there were lower values in the 45-year-old age group subjects.⁴⁰ The lack of significant changes in airflow measurements across the different age groups was attributed to slow adaptation and compensatory behavior. Similarly, in another investigation looking at “amplitude-based glottal airflow characteristics “ in 60 women stratified according to six age groups (10 in each group from 20–,30–,40–,50–,60–,70–) Sapienza and Dutka reported that none of the airflow measures used, namely, “minimum glottal airflow, alternating glottal airflow, peak glottal airflow and minimum glottal airflow,”⁴¹ was predictive of age.⁴¹ However, other investigators described significant differences in glottal resistance and airflow rates in elderly compared to young subjects. The study by Hodge et al on the mechanism for intensity difference between elderly and control subjects demonstrated lower values for sound pressure level and peak airflow, and higher open quotient in the elderly.³² In an investigation by Melcon et al on laryngeal valving in 60 men of different age groups, the authors reported lower mean airway resistance during sustained vowel production in elderly men (75 years old) compared to younger men.⁴² In another study by Holmes et al on subjects of different age groups, including 10 males and 10 females, the authors investigated laryngeal airway resistance (RLAW) at four sound pressure levels (SPL). The results indicated significant difference in RLAW values at all sound pressure levels in women compared to men and in women across different ages, in addition to a significant difference between the oldest male group and the youngest at the 75th SPL percentile. The authors also reported “more linear changes in transglottal airflow and transglot­tal pressure as relative SPL increased in men.”⁴³ They concluded that women, unlike men, seem to have less speech intensity variations, probably secondary to the high laryngeal airway resistance attributed to relatively small laryngeal size.

Stroboscopy, Electroglottography, and High-Speed Imaging in the Elderly

In parallel with all the aforementioned perceptual, acoustic, and airflow alterations in the elderly, vocal folds changes are often observed on laryngeal examination. The most common laryngeal stroboscopic findings are vocal process prominence, bowing of the vocal folds with incomplete closure, vocal fold edematous changes, stiffening, reduced pliability of the vocal fold cover, irregular vibratory behavior, and aperiodicity.^{19, 44–48} In the study in 1980 by Honjo and Isshiki, the authors reported evidence of vocal fold atrophy and edema in men and vocal fold edema in women.¹⁹ Similar results were reported by Linville et al in a group of 20 elderly women.⁴⁴ However, they found vocal fold edema and inadequate glottic closure but in different frequencies in comparison to the report by Honjo and Isshiki in 1980.⁴⁴ A few years later, Linville, in her investigation on glottal gap configuration in relation to loudness and pitch, reported significant differences between elderly and young women. The young group displayed a posterior chink more often on stroboscopic examination, whereas elderly displayed more anterior gap with a spindle-shaped opening.⁴⁵ In another study on elderly women by Biever and Bless in 1989, stroboscopic examination revealed incomplete closure, vocal fold edema, and aperiodicity with alterations in both mucosal wave and amplitude.⁴⁶ Pontes et al examined the correlation between presbylaryngeal glottic signs of aging and vocal characteristics in 88 men and 122 women. The authors reported the prevalence of membranous spindle-shaped chinks in 37.6%, vocal process prominence in 29.5%, and vocal fold bowing in 23.8% of the total group.⁴⁷ Similarly, Pontes et al in their analysis of the senile larynx have reported significant differences in the prevalence of vocal process prominence in females (56 vs 8, p-value 0.0006) and a significant difference in the prevalence of vocal fold bowing in males (68 vs 0, p-value less than 0.0001) compared with younger subjects. The analysis was conducted on 100 laryngeal images taken from 50 elderly subjects compared with younger subjects (65–85 years) with no vocal complaints.⁴⁸ Likewise, in a study on 361 elderly, Takano et al reported the presence of vocal fold atrophy in 20% of the cases in his review of 361 patients (47 men and 25 women) above the age of 65 years. The authors demonstrated also a negative correlation between maximum phonation time and age, and a positive correlation between mean airflow rate and age.⁴⁹ Interestingly, the degree of vocal fold bowing seen during abduction does not always correlate with the glottal opening seen during phonation.⁵⁰

Other diagnostic modalities such as electroglottography and high-speed laryngeal imaging confirm the presence of glottic changes in the elderly. Electroglottographic analysis often reveals an increase in the open quotient for vowels that correlate with the perceived age of the speaker. For example, Winkler and Sendlmeier showed an increased open quotient on vowels in elderly men, which correlated with perceived age.⁵¹ In a study by Yamauchi et al using high-speed imaging in 46 elderly patients with vocal fold atrophy, the authors reported “larger open quotient, larger lateral phase difference, larger glottal width and smaller speed index” in comparison with a group of vocally healthy controls.⁵²

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