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Aging Clin Exp Res (2014) 26:1–5

DOI 10.1007/s40520-013-0143-5

REVIEW

Aging voice: presbyphonia


Regina Helena Garcia Martins • Tatiana Maria Gonçalvez •

Adriana Bueno Benito Pessin • Anete Branco

Received: 5 May 2013 / Accepted: 5 September 2013 / Published online: 26 September 2013
Ó Springer International Publishing Switzerland 2013

Abstract Presbyphonia is a physiological process of clinical, physiopathological, histopathological, vocal ana-


aging voice that includes morphological changes in the lysis, and treatment aspects.
coverage mucosa, muscle, and cartilage. We revised the
morphological, endoscopic, and vocal acoustic changes Physiopathology of the vocal production and structural
that occur in presbyphonia and discussed some treatments characteristics of the larynx in the aged
proposed to minimize glottal incompetence and improve
vocal performance of the elderly. The pathophysiology of vocal production involves three
systems: respiratory, vibrator, and resonator. In the respi-
Keywords Presbyphonia  Voice  Elderly  ratory system, the expiratory air is produced from the lungs
Dysphonia  Aging and passes between the vocal folds making them vibrate.
Diseases that compromise the vital lung capacity, reduce
the intensity of the voice. The vibrator system corresponds
Introduction to the structure of the vocal folds and the resonator system
to the supraglottic, the hypopharynx, the nasopharynx, and
Senility process does not spare the laryngeal structures, and the oral cavity. Thus, vocal production depends on the
the sequence of physiological events related to voice aging pulmonary aerodynamic mechanism, myoelastic structures
is named presbyphonia, which includes morphological of the larynx, laryngeal mucosal wave, and resonance
changes in its coverage mucosa, as well as muscle, carti- channel [3]. Optimal voice (euphonia) is the result of a
laginous, neurological, and functional alterations [1, 2]. We well-controlled air flow produced by the pulmonary sys-
reviewed the main research manuscripts available at the tem, a regular mucosal wave along the entire vocal fold and
databases Medline, PubMed, EMBASE, Lilacs, SciELO, a proper resonance of the vocal tract.
and Cochrane, which address presbyphonia, considering The pioneer studies of Hirano introduced the concept of
body-cover to the structure of the vocal fold and the tri-
laminar configuration of the lamina propria, dividing it
into superficial, intermediate, and deep layers [4]. Epi-
R. H. G. Martins  T. M. Gonçalvez  thelial structures are related to the cover while the vocal
A. B. B. Pessin  A. Branco muscle is related to the body and both of them have a
Department of Otorhinolaryngology, Botucatu Medical School, dissociate participation during the muco-ondulatory
São Paulo State University, Botucatu, São Paulo, Brazil
movement [5]. The larynx undergoes a continuous process
R. H. G. Martins (&) of growth and differentiation from birth to the adult age.
Disciplina de Otorrinolaringologia, Departamento de The structures of the lamina propria gradually differenti-
Oftalmologia, Otorrinolaringologia e Cirurgia de Cabeça e ate, even though an outline of vocal ligament can be
Pescoço, Faculdade de Medicina de Botucatu, São Paulo
recognized already at birth [6]. However, the true tri-
State University, Distrito de Rubião Junior s/n, Botucatu,
São Paulo 18618-970, Brazil laminar configuration of the lamina propria can only be
e-mail: rmartins@fmb.unesp.br noticed from adolescence.

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Among the compounds of the lamina propria are fibro- Videolaryngostroboscopic findings
blasts, elastic and collagen fibers, glycoproteins, hyaluronic
acid, proteoglycans, glucosamines, and rare capillaries. Videolaryngoscopy of the presbyphonia reveals vocal folds
Hyaluronic acid, an important compound of the extracel- bowed and with marked concavity of its free edge due to
lular matrix, is responsible for the local regulation of the atrophy of the vocal muscle (Figs. 1, 2). The video-
water content, reducing the impact of phonotrauma [7]. laryngostroboscopy shows aperiodicity of the glottic cycle,
The intermediate layer of the lamina propria is rich in decrease in the glottic wave amplitude, and reduced phase
elastic fibers and the deep layer, in collagen fibers. Colla- of glottic closure. Sulter et al. [18] assessed 214 video-
gen fibers are responsible for maintaining the tension and stroboscopies of aged people and noted that the vocal folds
the stretching of vocal folds, while elastic fibers play the were thicker, vertically longer and laterally denser with
role of rapidly correcting the organ when the latter is less muco-ondulatory movement amplitude in men, relative
exposed to deformities [8]. Type-I collagen is distributed to women. Glottic closure was more complete in men than
over the superficial layer, close to the basal membrane (thin in women.
fibers), the deep layer and the macula flava; type-III col-
lagen is found all over the lamina propria (thin and thick Clinical characteristics of presbyphonia
fibers), while type-IV and type-V collagens (fibrous com-
pound) are distributed over the basal membrane and The degree of vocal deterioration in presbyphonia is related
endothelium of vessels. Elastin, an important compound of to individual susceptibilities such as physical and psycho-
the extracellular matrix of vocal folds, is found in maculas logical health, life habits, and racial and hereditary factors
flavas, superficial (very close to the basal membrane),
intermediate, and deep layers [9, 10].
Morphological studies of the senile larynx have sug-
gested that, besides the decrease in the quantity of elastic
fibers, there are morphological changes that compromise
their function, including the increase in amorphous sub-
stance, the decrease in myofibrils, and the changes in their
metabolism [11]. Ohno et al. [12, 13] attributed the fall in
the phonatory intensity of the aged to the reduced density
of the extracellular matrix, a result of increased collagen
and decreased hyaluronic acid. Ximenes et al. [14] con-
ducted a histomorphometric analysis of larynxes of aged
people and noted that both the thickness of the lamina
propria of vocal folds and the density of epithelial cells
were reduced, and such changes were more evident in men.
According to those authors, these findings may justify the
vocal pattern observed in presbyphonia. Fig. 1 Atrophic vocal folds and vocal apophysis prominent
With aging, there is an increase in the relationship
between the numbers of collagen and elastic fibers result-
ing in higher rigidity and consequently decreased vibratory
wave of the vocal folds [15]. In parallel, there is a decrease
in the concentration of hyaluronic acid and mucus-pro-
ducing glands, also reducing the viscosity of vocal folds
[11, 16]. All these structural changes unfavorably affect the
voice performance of the aged. In elderly women, the
fundamental frequency (f0) decreases and the vocal
symptoms become more frequent.
In addition to structural changes in the epithelium and in
the lamina propria, the senile larynx may undergo calcifi-
cation of hyaline laryngeal cartilages, atrophy of muscles,
including the vocal muscle and decreased transmission and
failure in the neuromuscular control. The latter changes
result in instability and vocal tremor, constituting a marked
characteristic of the voice of the elderly [3, 17]. Fig. 2 Atrophic and bowed vocal folds

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[3]. The most relevant vocal symptoms are vocal fatigue, dysphonia, are systemic lupus erythematosus, rheumatoid
hoarseness, difficulty in singing and in voice projection, arthritis, and Sjögren syndrome. In these diseases, dys-
cough, increased secretion in the airways, and decreased phonia may affect 30–38 % of patients [24]. In rheumatoid
vocal intensity [19]. Age-related vocal changes are so arthritis, bamboo nodes are in the mid third of vocal folds
marked that they easily reveal the age of the person to like yellowish nodular lesions, compromising the vocal
whom we are talking to on the telephone, only by hearing performance. These laryngeal lesions are histologically
their voice. For voice professionals, the vocal changes that similar to subcutaneous rheumatoid nodules [25].
occur in presbyphonia may culminate in early interruption Some drugs can also damage vocal emission, such as the
of professional activities, as is the case for teachers. It must negative effects of antihistamines, due to mucosal drying
also be considered that a large number of aged people sing and mucus thickness; the chronic cough caused by anti-
in choirs and alterations in their vocal quality may limit hypertensives, specially the angiotensin-converting
their performance, depriving them from moments of enzyme [26]; the dysphonia caused by chronic use of
relaxation and leisure [20]. inhaled corticosteroids, reported by 5–58 % of the asth-
Elderly singers frequently report reduction in their voice matic patients, due to laryngeal injuries, myopathy,
range and vocal training has helped them to delay the vocal inflammation, edema or moniliasis.
deterioration of presbyphonia. Prakup [21] showed the In addition, auditory changes are commonly observed
benefits of training the voice during the study of differ- among the aged, which impairs the feedback of the voice
ences in the vocal acoustic measures (f0, jitter, intensity, intensity control; programs for adaptation of individual
and shimmer) of older amateur singers (30 males and 30 hearing aids have minimized such damages and improved
females) and non-singers (30 males and 30 females). The the life quality of this population. The aged also show tooth
results of this study indicated that male and female singer loss which considerably interferes in the articulation,
participants were perceived to be significantly younger impairing the speech intelligibility.
than male and female non-singers. Singers had less jitter
and greater intensity than non-singers. Auditory perceptual and acoustic characteristics
Aging also evolves with a decrease in the production of of presbyphonia
secretions. There is a decrease in salivary secretion and
mucous glands, and consequent thickening in the secretions Auditory perceptual voice analysis shows decreased har-
of the pharynx and the larynx, making the vocal folds less monics and vocal range, tremor, reduced speech rate,
lubricated and damaging the vibration of their mucosae. In increased degree of breathiness, lack of pneumophonic
these cases, the ingestion of a large amount of liquid, coordination, and reduced vocal intensity and maximal
around eight glasses per day, is recommended to minimize phonation time. In some cases, there are variable degrees of
these symptoms [22]. excessive nasal resonance.
The voice is also influenced by emotional factors, and The investigation of perceptual vocal characteristics is
feeding habits and vices. Smoking causes a chronic usually carried out by speech therapists who adopt the
inflammatory process and triggers a series of structural GRABASI scale for this purpose. In this scale, each letter
changes that compromise both the epithelium and the corresponds to one analyzed vocal parameter: overall grade
lamina propria of vocal folds, culminating in the estab- or severity (G), roughness of the voice (R), breathiness (B),
lishment of permanent lesions such as Reinke’s edema, asthenia (A), strain (S), and instability (I). The degree of
leukoplakia, pachydermia, mucus thickening, and even intensity of each parameter is quantified as 0 (without
carcinoma. alteration), 1 (mild alteration), 2 (moderate alteration), and
Presbyphonia is a multifactorial phenomenon and other 3 (severe alteration). Gama et al. [27] analyzed the voices
comorbidities related to vocal change such as metabolic, of 103 aged people without vocal symptoms (aged between
autoimmune, and neurological diseases should be investi- 60 and 100 years) by GRBASI scale and noted significant
gated. These diseases are more common in the elderly and changes in the vocal parameters for 44.66 % cases, espe-
thus must be identified, diagnosed, and duly treated or cially concerning roughness, breathiness, and instability.
controlled for a successful vocal therapy. Disorders of the Asthenia and tension were the least affected parameters.
thyroid gland may damage the voice both in hyperthy- Computerized acoustic analyses have indicated a
roidism and in hypothyroidism. In hyperthyroidism, there decrease in the fundamental frequency of women and an
may be dystonias, paradoxical movements, and laryngeal increase in that of men, as well as increased percentage of
tremors; in hypothyroidisms, there is edema of vocal folds jitter and shimmer [27, 28]. Gama et al. [27] evaluated the
and the voice can become weak with decreased funda- acoustic measures of voice for 96 women aged between 60
mental frequency and vocal range [23]. Among the auto- and 103 years and found a significant and gradual reduc-
immune diseases of the elderly, which may evolve with tion in f0 for aged women, from 193.81 Hz for 60 years to

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187.60 Hz for 80 years. For some women older than long-term vocal restoration. Hyaluronic acid stimulates
80 years, those authors recorded f0 values close to 88 Hz. connective tissue formation, presents a similar viscosity of
the vocal fold mucosa and can be useful [32]. Even though
new biomaterials have arisen and indications have been
Treatment for presbyphonia improved, injectable materials require attention as to tol-
erance, location of the substance-receptor site, reabsorption
Vocal therapy degree, and viscosity.
A frequently used and long-lasting technique for glottic
Voice rehabilitation in presbyphonia contemplates the insufficiency is the graft of fascia or pre-fascia of the
improvement in oral communication, with decreased temporal muscle; it is easy to obtain and accommodates in
speech effort, fitting the vocal quality to the needs of the the lamina propria, promoting little reabsorption over the
aged. Vocal exercises have been proposed to favor the years [33].
glottic closure, increase the subglottic pressure and the Type-I thyroplasty is reserved for more severe cases of
voice intensity, stabilize the vocal quality and the funda- glottic incompetence in which breathiness is very impor-
mental frequency, and provide a global improvement in the tant, as is the case for laryngeal paralysis. This technique
speech functional system. Vocal therapy may improve requires external cervical approach and introduction of
voice quality, maximal phonation time, pneumophonic silicon mold into a window made in the thyroid cartilage
coordination, tension, articulation, velocity, intensity, res- [34].
onance, pitch, and vocal attack, depending on the aim of With the advance of knowledge of the microstructure of
the rehabilitation [29]. vocal folds, fibroblast culture has been cited as a future and
Vocal therapy should start with exercises for respiratory promising method to treat glottic insufficiency; on the other
support, resonance control, and supraglottic hyperfunction hand, current studies are still premature and do not include a
exercises to improve the approach of vocal folds [30]. follow-up. In addition, the culture methods are not totally
Vocal education should include optimal vocal postures, standardized yet, especially concerning the culture time and
neuromuscular coordination, respiratory exercises, and the grafting interval. Hirano et al. [35] described the first
practice on resonant voice production. Most patients are technique for fibroblast implantation in humans; they
benefited by these vocal therapies. Failures in vocal reha- injected 10 lm culture in the left vocal fold, under topical
bilitation are usually found in patients with important vocal anesthesia. Based on videostroboscopy and acoustic and
fold atrophy and those with systemic diseases. Mau et al. aerodynamic parameters, after 3-month follow-up, those
[31] analyzed the results of vocal reeducation treatment of authors noted that the vocal fold atrophy improved, the
67 patients older than 55 years and noted that 85 % of glottic aperture disappeared and the acoustic and aerody-
these patients demonstrated improvement with voice ther- namic parameters were normalized. The authors have a
apy. Patients with pronounced vocal fold atrophy presented special interest in studies involving fibroblasts because these
less improvement from voice therapy. cells are essential compounds of the lamina propria and
However, when surgery is necessary, the patients may responsible for the maintenance, development and repair of
benefit from a postoperative voice therapy follow-up aimed the extracellular matrix. The metabolic activity of fibro-
at maximizing the laryngeal function, maintaining an blasts seems to decrease with aging, showing changes in
adequate vocal quality and guiding patients in ceasing their cytoplasm organelles. The most evident alterations are
habits that are harmful to the voice and adopting preventive in the rough endoplasmic reticulum, responsible for the
strategies. synthesis and storage of proteins, and in the Golgi apparatus,
responsible for storing, processing and distributing proteins
Surgery and polysaccharides [12, 13]. Further studies are needed to
prove the benefits of these new therapeutic techniques for
Several materials like teflon, collagen, hyaluronic acid, fat, the lamina propria repair by adopting these methods.
and geofoam have been employed for the correction of the
glottis incompetence; however, the ideal substance to be
injected inside the vocal folds is still under investigation. Conclusion
These substances have been used in laryngeal scars and
vocal sulcus, inducing minor inflammatory response. Tef- We revised the morphological, endoscopic, and vocal
lon injection has shown limited results for the susceptibility acoustic changes that occur in the presbyphonia. We dis-
to granuloma formation. Fat injection has shown rapid cussed some treatments that have been proposed to
absorption and suggested not to be a good choice for improve vocal performance of the elderly.

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Conflict of interest On behalf of all authors, the corresponding 17. Paulsen F, Kimpel M, Lockemann U, Tillmann B (2000) Effects
author states that there is no conflict of interest. of ageing on the insertion zones of the human vocal fold. J Anat
196:41–54
18. Sulter A, Schutte H, Miller D (1996) Standardized laryngeal
videostroboscopic rating: differences between untrained and
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