DOI: 10.31038/SRR.2019212

Abstract

Objective: To determine whether the vocal folds length, along with the acoustic voice parameters measurements, can predict the moment of upcoming voice mutation and assess the process of a child’s maturation.

Study design: A cohort study started with examination of children at a premutation age, and a follow up 2.5 and 5 years later.

Setting: Referral center (Claros Otorhinolaryngology Clinic)

Subjects and methods: Children at a premutation age were examined, with a follow up at a mutation and postmutation age. During each visit a CT examination was performed to determine vocal folds length, followed by an examination of the acoustic voice parameters and a videolaryngoscopy and videostroboscopy. Obtained values were analyzed statistically to find the correlations between them and the reported age of mutation.

Results: 50 children (25 males aged 11.5, and 25 females aged 9.5, with a follow up 2.5 and 5 years later) were examined. A study started with 73 children, but 23 of them failed to attend the first or second follow up. Statistical significance was reported for a correlation between the age of mutation and loudness in boys aged 14 (r = 0.48, b = 0.31), vocal folds length in boys aged 14 (b = – 2.18), and loudness in boys aged 11.5 (b = -0.15); and for girls for a correlation between the age of mutation and decrease of fundamental frequency between ages 9.5 and 12 (r = 0.5, b = 0.01).

Conclusion: The parameters mentioned above have a correlation with the moment of mutation and might in future become an additional way of evaluating a child’s development.

Keywords

Voice mutation, Voice break, Vocal fold length, Voice acoustic parameters, Child’s development

Introduction

Proper development in a child can determine his/her educational, professional and emotional future. We watch carefully during child’s growth if this process is not disturbed. However, it is not easy to evaluate; especially during puberty, which is unique to every child and is determined by such an unpredictable and complex factor as the game of hormones [1]. Many authors agree that, while assessing the moment of puberty in girls is easy because of the presence of menarche and breast growth, it is more difficult in boys because of a lack of these concrete breaking moments and its extended character [2, 3]. It is well known that, in contrast, the situation is opposite with respect to mutation; i.e. it happens in a much more subtle way for girls, whilst for boys mutation happens suddenly, more dramatically, and more noticeably [2, 4, 5]. The interesting phenomenon of voice break during puberty has tempted many authors to evaluate the development of a child by assessing the age of voice break as a clean sign of puberty.^{1, 6, 7} Although exploring the subject of mutation by evaluating the acoustic parameters of the voice has received a reasonable amount of attention in the literature [6, 8–11], the other ways of predicting the time of mutation, especially by examining the length of vocal folds based on CT scans, are to the best of our knowledge underexplored. We conducted our research to address this gap.

Our Clinic is a widely known consultancy for professional opera singers of the Gran Teatro del Liceo in Barcelona, specializing in the issue of voice since 1970, and also providing medical support for a large number of Spanish children. The medical data presented in this article is the result of our work over the past five years. The objective of our research was to establish correlations between the change of vocal folds length and acoustic parameters and signs of voice break described by children and their parents, and therefore to determine which combination of parameters would be the best to evaluate a child’s development.

Changes in the vocal box over the growth of a child are the consequence of complex coordination between the respiratory, digestive and nervous systems [12], as well as anatomical, histological and neurological modifications [13]. In comparison to the adult larynx, the pediatric larynx has disadvantages in voice production on an anatomical level [4], insofar as the ratio of the membranous vocal fold length to the total vocal fold length is lower, the cartilaginous framework is less rigid, and the incidence and degree of posterior glottic chink is increased [14]. Histologically, the pediatric larynx also varies a lot compared to the adult one, which manifests mainly in increased cellularity and decreased cellular differentiation and organization [15], as well as in the lamina propria which begins as a monolayer [16, 17], and changes into a bilayer around the age of 10 and into a trilayer after puberty [18]. Some authors argue that the triple structure of lamina propria occurs already at the age of 7 [4, 19], however, it is widely accepted that the distribution and composition of the collagen and elastic fibers do not mimick those of adults until puberty [15, 16, 18, 20]. Other differences in the pediatric larynx include elevated overall subglottic pressure and recruitment of a greater percentage of pulmonary capacity [4, 21], which changes during mutation.

The reason for these changes lies mainly in the histological structure of the vocal fold – female and male vocal folds alike express androgen receptors in the cytoplasm of the laryngeal gland, progesterone receptors in the nuclei of the same cells, and estrogen receptors in the epithelial cells of the larynx [4, 22, 23], leading to muscle thickening, final development of the trilayered lamina propria, changes in elastin and collagen deposition between the layers, variable lubrication and vocal fold elongation [24]. The expression of the receptors is similar for boys and girls, however differences in the level of hormones between genders causes differences in vocal fold development. In contrast, the other histological features vary: there is more elastin in the cover than in the ligament of male vocal folds, while the elastin in the female lamina propria is more compact [20, 25]. These differences lead to enormous distinctions in the male and female mutations. Apart from the difference in its dynamics, for girls, voice break happens earlier [26–28], starting from the age of 10 and finishing about the age of 14 years, whilst for boys it happens around the age of 12–16 years [29], with some period of voice instability [30, 31]. For both genders it results in the enlargement of arytenoids, expansion of the laryngeal muscles and ligaments [32, 33], completing of the glottal closure, lengthening of the framework of the larynx, and lengthening and rounding of the vocal folds, ⁴ which is highly related to changes of the acoustic parameters. It is important to note that nowadays mutation occurs much earlier than in the past [2, 34]. This was widely described by Daw, who recorded the age of voice break in members of J. S. Bach’s choirs in Leipzig in 17271749 as being 18 years old [35].

Materials and Methods

The study protocol was acknowledged, reviewed and approved by the internal ethics committee of our medical center, Claros Otorhinolaryngology Clinic Institutional Review Board. All of the parents and children were informed about the examination technique and provided written informed consent. We examined children of a premutation age, with a follow up 2.5 and 5 years later (at the mutation and postmutation age). Exclusion criteria were: vocal fold pathologies, history of neck trauma, previous intubations or laryngeal, head and neck or torso surgeries that have caused changes in vocal folds structure. For the power of a test equal to 0.9 (90%), the smallest sample size was calculated for each checked independent variable, and for statistically significant variables it varied from 10 to 41.

As advised by the pediatric voice assessment guidelines and European Laryngological Society (ELS), subjective and instrumental acoustic evaluations of the voice and aerodynamic performance, as well as visual evaluation of the larynx, were performed [36–38]. During each of the three appointments that the child attended, the voice parameters were measured by a speech- language pathologist. We chose these specific parameters based on advice from the literature: fundamental frequency as the basic, classical objective parameter of the voice [13], vocal range as quite a broad parameter, and because of that a strong sign of a voice disorder if pathological, shimmer and jitter as described as non-invasive, relatively easily applicable and objective [13, 39–41], and, furthermore, highly related to voice problems and dysphonia, [36, 42–44] loudness because it is believed to be a necessary parameter to objectify the result of checked jitter and shimmer [39, 45, 46], and maximum phonation time because it is believed to be the simplest, most easily measured aerodynamic parameter of phonation [47]. To perform the examinations we used sustained vowels taking examples from the approved authors [13, 39, 48, 49]. The vocal recording was performed in accordance with the Union of European Phoniatricians recommendations, with the child in a standing position, in a silent room, with noise level no higher than 40 dB, and with a microphone placed in front of the mouth at a 30 cm distance [50]. We used a microphone from Bruel & Kjaer Rhino-larynx Stroboscope—Type 4914 (Bruel & Kjaer Sound & Vibration, Denmark). All children were examined and recorded in the same conditions. Based on approved literature we defined the norms of all checked parameters [47, 51–59], and we compared them to obtained values. Finally, an ENT consultant examined the vocal folds during every visit to exclude any pathologies, performing a videolaryngoscopy with a rigid endoscope followed by a videostroboscopy (Hopkins II telescope 70 degrees, Karl Storz, Germany).

On every single visit, every 2.5 years, after parents and children provided written informed consent again, CT scanning was performed the way confirmed to be accurate before in our different study [60], using Philips Brilliance ICT 256 (Medical Systems, Netherlands), in the supine position, from the level of the frontal to the level of the aortic arch. Acquisition parameters consisted of a tube current—250 mA, 120 kV, 128×0.625 detector collimation, 0.75-second rotation time, pitch 0.993, scan field of view of250, standard resolution, raw slice thickness – 1 mm. For laryngeal evaluation we added a set of axial reconstruction 2×2 angled through C4 C6 disc spaces. The reconstruction interval was 0.5 mm and the slice thickness was 1 mm. Using standard CT software, a radiologist measured the precise length of the vocal folds in the axial view of the glottis, the longitudinal size of the glottis was estimated in a midsagittal plane (from anterior to a posterior boundary), and in the axial plane, and the length of vocal folds was measured between the anterior commissure and the most posterior part of vocal folds.

Finally, after the third examination (five years after the initial one), the children and their parents answered a survey. The first questions included gender, current age and presumed age of mutation. The following parts of the survey included questions about signs of mutation and voice problems during voice break. The next set of questions related to the age of menarche and breast growth for girls and the age of the first signs of puberty for boys. Lastly, they were asked to complete with the speech-language pathologist the GRBAS scale, which gives scores from 0 to 3 for hoarseness, roughness, breathiness, asthenia, and vocal strain [61].

Data was then implemented into Statistica 13.1 (StatSoft Poland, Cracow) software. Statistical significance was reported at the alpha level of 0.05. P value below 0.05 was considered significant. While analyzing the data we performed the Pearson correlation coefficient test, as well as an analysis of multiple regression and simple linear regression. Correlation coefficients were interpreted to determine whether the effect size was low (correlation coefficient-O.lO), medium (correlation coefficient~0.30) or high (correlation coefficient~0.50). Hypothesis tests were designed as two-tailed. A hypothesis null was formulated as HO: there is no correlation between the change of vocal folds length or acoustic parameters and the moment of voice break (r = 0, b = 0), against the alternative hypothesis H1: there is a correlation (r≠0, b≠0). We created graphs and classification trees to present our findings. The power of the test was determined, and the confidence intervals (Cl) were established for the obtained values.

Results

50 children of a premutation age were our final study group (25 males and 25 females) with a follow up 2.5 and 5 years later (in the mutation and postmutation age). Exactly half of them were males examined at age 11.5, age 14 and age 16.5, and the other half were females examined at age 9.5, 12 and 14.5.

While analyzing the correlations between all the obtained variables and the age of mutation with the Pearson correlation coefficient test, we reported statistical significance in the correlation between the age of mutation and loudness in boys aged 14 (positive correlation coefficient r = 0.48, 0.48, 95%, CI:0, 10–0.73, P = .015, power of the test = .7). Multiple regression analysis showed statistical significance in the correlation between the age of mutation and vocal fold length in boys aged 14 (negative coefficient b = -2.18, P = .044), as well as loudness in boys aged 11.5 (negative coefficient b = -0.15, P = .047), loudness in boys aged 14 (positive coefficient b = 0.31 , P = .022), and loudness in boys aged 16.5 (negative coefficient b = -0.31, P = .040\ however, loudness in boys aged 16.5 cannot be treated as a predictor of mutation, which presumably had occurred earlier). The effect size for these coefficients was R² = 0.88 (0.88, 95%, CI: 0.72–0.93) and the Cohen’s coefficient was f² = 7.33. Deeper analysis of these calculations is shown in the classification trees (Figures 1 and 2).

Figure 1. Classification tree for loudness in boys aged 11, 5, loudness in boys aged 14, loudness in boys aged 16.5, and vocal folds length in boys aged 14.

Loudness in boys aged 14. and subsequently vocal folds length in boys aged 14, differentiate cases the best. Combined, they are a good prediction of the age of mutation.

Figure 2. Classification tree for all the values obtained in boys aged 11.5 and 14. In these age groups vocal folds length in boys aged 11.5 was the best parameter differentiating cases

In the same calculations for girls, we reported statistical significance in the correlation between the age of mutation and the age of first menstruation (positive coefficient r = 0.84, 0, 84, 95%, CI:0, 66–0, 92, P<.001. power of the test = 1) and increase of fundamental frequency between the age of 9.5 and 12 years old (negative coefficient r = -0.5, 0, 5, 95%, CI:0.13–0.74, P = , 011, power of the test = .75). Since the correlation coefficient between the age of the mutation and the age of the first menstruation was high, we could perform an analysis of simple linear regression, results of which are shown in Figure 3. Multiple regression analysis also showed a statistically significant correlation between the age of mutation and the age of the first menstruation (positive coefficient b = 0.7, P<.001). and increase of fundamental frequency (negative coefficient b = -0.01, P = , 039), which is in agreement with previous calculations. The effect size for these coefficients was R² = 0.76 (0.88, 95%, CI:0.54–0.86) and the Cohen’s coefficient was f² = 3.1. Further analysis is shown in the classification trees (Figures 4 and 5).

Figure 3. Scatterplot showing analysis of simple regression and a prediction zone of 95% for the mutation age. We can see that, e.g., for the menstrual age of 12 (axis x), with 95% of probability the mutation will occur between the age of 11.8 and 13.2 (axis y).

Figure 4. Classification tree for the values obtained in girls aged 9.5, 12 and 14.5. Age of the first menstruation was the best parameter differentiating cases in respect of the mutation age.

Figure 5. Classification tree for the increases of the values obtained in girls between ages 9.5 and 12. Age of the first menstruation was the best parameter differentiating cases.

Discussion

The main aim of our study was to find the parameter which correlates the best with the age of mutation, and therefore could possibly serve to predict the age of mutation and evaluate development of the child. We took under further considerations only the values with confirmed statistical significance.

With respect to boys, our calculations showed a statistically significant correlation between the age of mutation and loudness in boys aged 14. vocal fold length in boys aged 14, and loudness in hoys aged 11.5. For loudness in hoys aged 14 the correlation coefficient was positive, which tells us that the louder a child sings at the age of 14, the later he has the mutation. For loudness in boys aged 11.5 and vocal fold length in boys aged 14 the correlation coefficient was negative, which tells us that the louder boy sings at the age of 11.5, the lower the age of mutation, and – most importantly – the longer vocal folds are at the age of 14, the sooner the mutation will start. This is especially interesting in the case of boys, because despite of the obvious vocal folds lengthening with age, male mutation is well accepted to be a sudden and steep change, [2, 4, 5] with periods of higher voice interrupted by periods of lower voice, [30,31] and is dependent on numerous systematic changes described above, therefore it is not simply related to the change of vocal folds length.

It is worth emphasizing, that the correlation between the age of mutation and loudness in hoys aged 14 was confirmed to be statistically significant by all the statistical tests that we performed, and also was the best value differentiating the cases in respect of the age of mutation in the classification tree (Figure 1), therefore it is a variable worth special attention.

Our study also revealed interesting findings in girls. The calculations showed a statistically significant negative correlation between the age of mutation and increase of fundamental frequency between the age of 9.5 and 12. Which means that the more fundamental frequency drops between the age of 9.5 and 12 years old, the later mutation occurs. We have also confirmed a statistically significant positive correlation between the age of mutation and age of the first menstruation. Which means that the sooner the first menstruation appears, the sooner the voice break starts. This is not a surprising result; however, it gave us the opportunity to deepen our statistical analysis. Figure 3 illustrates an analysis of simple regression and the prediction zone of 95% for the mutation age, which means it allows us to predict with 95% of probability the age of voice break knowing the age of menstruation. This way of illustrating the correlation has the potential to be extremely useful in everyday medical and choral practice. The effect size of our results measured by the correlation coefficients was high.

It is important to point out that we have to consider the possible lack of precision in radiological measurements, however it is worth noting that our CT examinations had especially high resolution parameters, and that the CT scans were analyzed multiple times, in different views and planes. A further limitation of our study might be uncertainty about the proper understanding of our instructions during the acoustic examinations (which uncertainty accompanies scientists in every study involving children [62]), however, the age of children involved in our study was not so low as to make this a major concern.

Although several studies have investigated the subject of mutation and ways of predicting it, there is still room to explore it further. Decoster et al. investigated changes in acoustic parameters in girls, however boys were not the subject of the study [2]. Hacki and Heitmiiller, as well as Boltezar et al., did address the subject of mutation, yet in relation to acoustic voice parameters, not vocal folds length [6, 31]. Similarly, numerous studies examined acoustic voice parameters in pediatric population, though other examinations, such as vocal folds length measurements, were beyond the scope of the research [8–11]. Rogers et al. evaluated vocal fold growth as a function of age in a large group of patients [7], however using measuring sticks in total anaesthesia, and emphasized that it might have lengthened the vocal folds [63]. There are several other studies investigating vocal folds length in relation to age, however measurements were performed post mortem, and therefore did not reflect the actual conditions of the living human being’s body [18, 64–67]. Hollien, similarly as in our study, has used radiological imaging; however he has used X-ray images, which are less precise than the CT scans used in our research [68]. Thus, we are tempted to claim that our research is original, and to the best of our knowledge explores aspects not addressed before, adding an important contribution to still not exhausted research about a child’s development and the subject of mutation.

Conclusion

In the academic pursuit of knowledge, evaluating the proper maturation of a child has a special place of a particular concern. This is unsurprising, given that childhood can determine the future of a young human being. However, as we are all different, it is also difficult to determine whether development is proper, and, at the same time, so easy to miss the red flags. Undoubtedly, the period of puberty is the most challenging, both for the human body, which goes through multiple changes, and for scientists, who try to establish reference points to make the evaluation of maturing easier. We believe this hunt is never finished. In the future, one way to asses this might be a routine examination of vocal folds length and acoustic voice parameters. Our study attempted to make our contribution in bringing this future closer.

Acknowledgement

The authors report no conflicts of interest. The authors report no financial and material support for the research and the work reported in the manuscript.

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DOI: 10.31038/SRR.2019211

Summary

Purpose and study design: The research aims to estimate the prevalence and characteristic symptoms of vocal fatigue in professional opera singers. Also, the paper is summary of many years of clinical experience with management of singers with vocal fatigue in Clarós Clinic. The research was designed as a retrospective observational study.

Material and method: In the group of 250 professional opera singers who were examined in Clarós Clinic in 10 years period, fifty-five cases of vocal fatigue were reported and evaluated. Among subjects were 21 men and 34 women. Mean age of participants was 46,78y (range 19–72 years old, standard deviation: 12.18 year). Representation of classical voice types was: 14 tenors, 5 baritones, 2 basses, 22 sopranos, 10 mezzos, 2 contralti.

Results: Prevalence of vocal fatigue in 10 years period in the study group was 22%. The three most frequent symptoms observed in the study group were: muscle pain (87.27%), muscle fatigue (76.36%) and diffuse sharp pain in the neck (70.37%). Statistical analysis showed significance only for the relationship between female opera singers and incidence of symptoms such as tremulous voice and muscle pain. All other symptoms were not statistically related to gender. Contradictory to expectations, application of anti-inflammatory drugs was statistically associated with the longer duration of the symptoms.

Conclusions: Vocal fatigue may be underestimated but is one of the most frequent problems encountered in the ENT practice that provides care for professional voice users. In the presented research, administration of anti-inflammatory drugs has not been associated with faster recovery from vocal fatigue.

Keywords

vocal fatigue, opera singers, treatment of vocal fatigue, retrospective observational study, the prevalence of vocal fatigue.

Introduction

Professional opera singers are considered to be the highest class artists among singers. In fact, they should be perceived as Olympian athletes when comes to quality and ability of their vocal folds. Exceptional singing is achieved by years of training and vocal regime. Unfortunately, the requirements set for the opera singers’ voice entail the unique susceptibility to vocal fatigue. The research reported fatigue to be a common complaint among professional voice users [1].

Vocal fatigue presents a challenge to research and clinical practice. Despite the amount data gathered on that matter, precise definition and guidelines are still not well established.

Unlike in case of muscle fatigue, the creation of the conditions that allow the investigation be far more difficult because of complicated mechanism of voice production. Many studies which attempted to induce vocal fatigue yielded a different and inconsistent result. In case of singing, the task is especially challenging because repertoire can vary significantly. Furthermore, aspect like frequency of the performance can play a role in the development of vocal fatigue. Some types of voice are particularly vulnerable, like a soprano. However, the data provided on the subject is anecdotal, obtained from clinicians’ experience instead of large case-control studies.

Mechanisms which underlay vocal fatigue are multifaceted. Titze listed some potential physiological and biomechanical factors that may contribute: fatigue of respiratory and laryngeal muscles, fatigue of non-muscular tissues of the larynx, and changes in vocal folds’ viscosity [2]. As one of the others, the neuromuscular fatigue express inability of muscles to sustain the tension under repeated stimulation [3].

The exceptional ability of the larynx to produce sound is possible because of vocal folds which are covered with non-muscular, pliable tissue that generates multiple and rapid vibrations [4]. Furthermore, viscous properties of vocal folds epithelium allow lubrication and shock absorption [5]. Research showed that prolonged, high-pitched phonation could increase: frictional energy loss, heat dissipation and tissue viscosity. All these factors can lead to tissue fatigue [4]. The influence of tissue biomechanics on phonation makes the study about vocal fatigue more complicated than the research of fatigue involving other skeletal muscles.

The expression vocal fatigue has been applied and arbitrarily understood. For presented research, vocal fatigue definition was employed from Solomon as the self- report of an increased sense of effort with prolonged phonation, whether or not there are observable or measurable decrements in phonation function [5]. The aspect of self-reporting is particularly crucial amid opera singers who are the harshest judges of their vocal abilities.

Moreover, vocal fatigue has been described clinically by several authors. Common symptoms enlisted in literature were: husky vocal quality, breathy vocal quality, loss of voice, pitch breaks, inability to maintain regular pitch, reduce pitch range, lack of vocal carrying power, reduce loudness range, need to use greater vocal effort [1].

Opera singers are interesting subjects to study vocal fatigue because in comparison to other professional types of vocalists their vocal abilities are challenged at the highest level. Furthermore, years of vocal regime provide them with high self-awareness of the vocal capabilities which helps to notice any vocal problems at first onset.

Clarós Clinic provides medical support for a large number of professional opera singers of Liceu Opera theatre in Barcelona, Music Conservatory students and other singers since 1970’. Authors decided to analyse reports of vocal fatigue from last ten years among opera singers and describe common symptoms, frequency and interventions that were applied.

The research aims to determine the prevalence of vocal fatigue, symptoms and factors which may underlay the occurrence of that problem.

Paper is summary of our experience with treatment and management of vocal fatigue among professional opera singers.

Overall, vocal fatigue is still an intriguing and persistent problem when presented in clinical practice and is the challenge in the face of consequences which may cause for the professional singer with a tight schedule. Furthermore, the struggle with finding a substitute for a famous singer who suffers from vocal fatigue provides additional pressure for the clinician who has to offer effective treatment.

Materials and Methods

Study design

The research was designed as a retrospective observational study. Evaluation of vocal fatigue cases presented in Clarós Clinic during ten years period was conducted to obtain prevalence, symptoms and to analyse the treatment.

The research protocol was approved by ethics committee of Clarós Clinic medical centre.

Participants

In the group of 250 professional opera singers who were treated in Clarós Clinic in 10 years, fifty-five cases of vocal fatigue were reported and evaluated for this research. Among subjects were 21 men and 34 women. Mean age of participants was 46,78y (range 19–72 years old, standard deviation: 12.18 year). Representation of voice types was: 14 tenors, 5 baritones, 2 basses, 22 sopranos, 10 mezzos, 2 contralti.

Medical evidence

Eleven most common symptoms and six risk factors of vocal fatigue identified in the study group were gathered in Table 1.

Table 1. Common symptoms of vocal fatigue and risk factors with definitions.

Medical records were evaluated to search for possible causes and factor which may contribute to the development of vocal fatigue. Patients reported: overuse of voice, stress, incorrect technique, vocal warm-up, improper repertoire and shouting. Interventions which were used: voice rest regime, medications (anti-inflammatory drugs, steroids: hydrocortisone). Also, duration of the symptoms was measured. In some cases, the repetitive character of vocal fatigue was noticed.

 All cases of professional opera singers were presented to the same, senior, most experienced ENT consultant. He was responsible for the patient examination and evaluation. All medical records of patients with vocal fatigue were created by the senior consultant who followed the similar protocol in every case. Table 1 gathers the common symptoms and risk factors assessed in the study with the description of researcher interpretation.

In every case, the standard medical interview was gathered. Moreover, patients underwent ENT examination consisted of endoscopic evaluation and neck palpation.

A senior most experienced ENT consultant performed video laryngoscopy with conventional equipment to examine the vocal folds (Karl Storz® 70 degrees rigid endoscope and HD camera).

The table below shows typical symptoms and risk factors which were assessed in medical records. Description represents how researcher stated or understood given symptom or risk factor. Definitions were based on literature and authors experienced [3,6].

Statistical Analysis

Data was collected in Excel sheet and implemented to Statistica 13.1 (Statsoft) software for statistical analysis. Statistical significance was accepted at the alpha level of 0.05. A p-value below 0.05 was considered significant.

Contingency tables were used to analyse quality variable obtained from patients’ medical history. Percentage values for every symptom and risk factor were calculated for men, women and the complete group. The Chi² test was used to assess statistical dependence between gender and incidence of given symptom and risk factor.

Contingency tables were also implemented to analyse the possible influence of anti-inflammatory medication on the duration of symptoms.

Due to the qualitative nature of the data obtained from medical history more complicated analyses were not possible.

It needs to be to highlight that some types of voice are very infrequent which influence the precision of statistical analysis. In this study, the contralti, basses and countertenors occurred in the minority.

Results

The results section is divided into two parts: descriptive data (tables and chart) and the statistical analysis. The precise characteristic of descriptive data obtained from medical history is presented in table 2, 3 and 4. Percentage values of symptoms incidence are illustrated in Chart 1.

Chart 1. Bar chart. Percentage value of symptoms’ incidence.

Table 2.
Common symptoms of vocal fatigue in the study group.

The table shows the percentage of VF occurrence and percentage of cases in which medications were applied in the groups. The results of the Chi² test for independence between enlisted factor and gender are also given. Significance was reported at p-level below 0.05. None of given factors had gender predilection in the presented group.

Table 3. Risk factors of vocal fatigue analysed in the study group.

The table shows the percentage value of risk factors incidence in the groups and results of the Chi² test for independence between enlisted factor and gender. Significance was reported at p-level below 0.05. None of given risk factors had gender predilection in the presented group.

Table 4. Percentage value of vocal fatigue reoccurrence.  Percentage of cases in which anti-inflammatory medication was applied.

The Chi² for Independence test was used to assess the relationship between gender and vocal fatigue symptoms. Results of the Chi² test are also given in tables 2, 3.

Table 5 presents the percentage values of vocal fatigue recurrence among different types of classical voices.

Table 5. Recurrence of vocal fatigue among different voice types (tessitura- defined as most acceptable and comfortable vocal range for the given singer [28]).

The table shows the percentage value of risk factors incidence in the groups and results of the Chi² test for independence between enlisted factor and gender. Significance was reported at p-level below 0.05. None of given risk factors had gender predilection in the presented group.

The table presents the percentage of vocal fatigue reoccurrence among different voice types. In presented data sopranos and tenors were most frequently affected by the reoccurrence of VF. Examined contralti and basses had not experienced vocal fatigue more than one time at the moment of evaluation.

The chart shows the percentage value of symptoms which occurred in the whole group (general), men and women groups. Bars help to illustrate which symptoms were most common and compared them between groups. Therefore, three most frequent symptoms were muscle fatigue, diffuse sharp pain and muscle pain. Most common symptom among women as well as in men was muscle pain.

Results – Summary

The Clarós Clinic provided medical support for 250 professional opera singers during the time that the data was gathered. Symptoms of vocal fatigue were reported in 55 operatic vocalists, and these cases were enlisted to the research.

Prevalence of vocal fatigue in 10 years period among opera singers examined in the Clinic was 22%.

The three most frequent symptoms observed in the study group were: muscle pain (87.27%), muscle fatigue (76.36%) and diffuse sharp pain (70.37%). Most frequent complaints were pain-related, especially in female singers group.

Most common vocal complaints were: whispery voice (63.64%) and hoarseness (61.82%). More than a half of opera singers (52.73%) had difficulties with maintaining the vocal pitch during singing and quarter (21.82%) noticed changes in vibrato

The Chi² test showed statistical significance only for the relationship between female opera singers and incidence of symptoms such as tremulous voice and muscle pain (test Chi²: p = 0.037, p = 0.026). All other symptoms were not statistically related to gender.

Most common risk factors were: muscle overstain and overuse of voice which were present in over 80% of cases. Much less frequently, singers reported incorrect technique and inadequate repertoire as contributors to vocal fatigue (table 3).

Recurrence of vocal fatigue was noted in one-third of the singers and was more distinctive for female singers, especially sopranos and mezzo-sopranos (table 4).

Mean duration of the symptoms was 3.8day (standard deviation: +/- 1.9day). The median value was 3 day.

Contingency tables were also used to estimate the relationship between duration of the symptoms and application of anti-inflammatory medications. Results of the Chi² test showed that shorter length of the symptoms was related to lack of administration medication (test Chi²: p = 0.009).

Discussion

Vocal fatigue is an interesting and often debilitating condition, affecting many professional voice users. It gained much attention in the field of research, yet mechanisms which underlie the onset of this condition and its pathophysiology are still not fully understood. The amounts of vocal effort and specific elements which can trigger vocal fatigue are part of the ongoing debate. More research has to be done to develop reliable guidelines for management and treatment of vocal fatigue.

Every group of professional voice users have its characteristic which helps to study individual exposure factors. Opera singers have the individual susceptibility to fatigue which may interfere with social and occupational functioning.

The purpose of this study on vocal fatigue in opera singers was to state prevalence, characterise symptoms of this condition and review management.

Prevalence of vocal fatigue in studied group was 22%, which suggests that it might concern every fifth singer. As previous research showed among other types of professional singers, VF can cause voice impairment even more often. In a study conducted on the large group of various kinds of singers (opera singers- 49.8%), Phyland reported that participants experienced vocal fatigue in the previous year in 69% of cases [7]. In the research, fatigue was the second most frequent problem reported by singers after hoarseness [7].

Among most common symptoms reported by opera singers in the study group: two were pain related. Over 87% of singers pointed out the muscle pain as a single most common symptom of vocal fatigue. Female opera singers tended to suffer more from muscle pain than male singers, which was also confirmed statistically significant. Muscle pain was usually localised in throat, jaw and neck, but also in chest and back. These findings were consistent with previous reports which stated that most common pain present in singers were a sore throat (66%), pain during speaking (41%) and neck pain (35%). However, the study mentioned above pointed out the tendency for a sore throat among male vocalists, other types of body pains had no difference according to gender [8]. The presence of pain can severely compromise singer’s performance and negatively influence the quality of life. An important factor which helps to prevent the muscle pain is the concern for proper technique and vocal rest regimen.

Neuromuscular fatigue has been widely investigated in the literature. It can be presumed that muscle of the respiratory and phonatory system can fatigue and contribute to the deterioration of phonation or the perception of increased vocal effort, especially during prolonged high-pitched phonation. Undoubtedly, the research showed that respiratory muscles are highly unlikely to experienced fatigue. More recent findings presented evidence from whole body exercise suggesting that respiratory muscle fatigue occurs only following constant high-intensity training [9]. This situation cannot occur during regular physical activity, even as challenging as prolonged singing.

The distinction between fatigue of skeletal muscle and phonation muscles is relevant, because of the different histological structure. The capability of a muscle to maintain contraction over an extended period is related to a distribution of different motor units within the muscle body. In case of the larynx, the vast majority of intrinsic laryngeal muscle have fatigue-resistant muscle fibres (type I and IIa) rather than fatigable (type IIb) [10]. More recent studies provide interesting data showing the even more complicated histological structure of human intrinsic laryngeal muscles than presented in animal models [10]. These facts help to explain why singers usually complain about fatigue of muscle and experience discomfort in areas primarily localised in throat, jaw, and neck.

One of the unique aspects is non-muscular tissue fatigue which represents mechanical exhaustion. Mechanical deterioration represents the amount of strain that material can tolerate before breaking down. The fatigue represents progressive structural damage that results from mechanical stress (force per unit) imposed by strain on the material. Titze reported in one of his research that non-muscular tissue fatigue could cause damage to the laryngeal mucosa, but the quantity and duration of the physical stress were uncertain [11]. The author also described tensile stress which is required for high pitch phonation as a most significant mechanical stress in vocal folds vibration [11]

 Tissue viscosity plays a role in response to mechanical stress because that feature refers to individual properties of vocal folds’ mucosa responsible for lubrication and shock absorption. Research demonstrated that viscosity highly depends on the systemic and superficial hydration of mucosa. Singers in a situation of reduced systemic hydration may be particularly prone to experience the vocal fatigue [12]. Factor as prolonged, high-pitched phonation without proper hydration can lead to stress and strain which placed on the tissue can provoke fatigue. Furthermore, the viscosity of vocal folds mucosa can be affected by the decreased humidity of environment as in case of oral breathing [13].

The more recent study confirmed positive influence of systemic hydration on perceptual parameters of voice quality in singers. The improvement was seen in higher fundamental frequency, less cycle to cycle variation in pitch, or longer phonation time, depending on the individual. Hydrated vocal folds allow for optimal vibration, increase ease of phonation and prevent structural damage to vocal to vocal folds mucosa [14,15,16].

Non-muscular tissue biomechanical properties which include mucosal viscosity plays a significant role in the development of fatigue. In presented study 1/3 of singers have suffered from problems related to tissue fatigue.

Further, changes in vibrato were observed in over 52% singers. These changes represent acoustic differences related to vocal fatigue and can seriously interfere with performance. In previous research, Titze noted that muscle fatigue results in decreased ability to maintain stable tension in vocal folds [2]. In another interesting study, Boucher attempted to isolate acoustic signs of fatigue in laryngeal muscles. The study showed that 12 conventional acoustic parameters that were measured neither demonstrated consistent linear relationships with the fatigue estimates. Though, average values demonstrated the consistent peaks in vocal tremor and appeared near the points of critical shifts in muscle fatigue. In sum, rises in tremor corresponding to shifts in muscle fatigue appear robust in the face of fluctuations in modal pitch [17].

A more recent study helped to differentiate the acoustic changes related to vocal fatigue. The research was the first to demonstrate a link between tremor and observed muscle fatigue that is specifically attributable to voice effort and not only to fatigue linked with waking hours. Also, the results do not support applications of F0 or other conventional acoustic parameters as manifestations of fatigue in laryngeal structures. Even though many research showed significant rises in F0 as a result of vocal effort with reference to group averages, the recent reports showed that individual or cross-subject changes in F0, as in other conventional acoustic parameters do not consistently indicate fatigue in laryngeal structures [18].

Despite years of research, no consensus has emerged that could support the elaboration of guidelines for vocal fatigue. In the most basic approach, investigations on vocal fatigue have concentrated on identifying changes in voice in tests where fatigue was provoked by tasks of various “vocal load”. The assignments varied across different research; participants were asked to read or sing at varying pitch or intensities for a variable period extending from few minutes to several hours [19]. Those arguments make cross-study comparison useless with results on suggested vocal symptoms inconsistent and sometimes contradictory.

In our study as the first line of treatment, the vocal rest regime was applied in every case. Importance of vocal rest was underlined in many research and is usually required as first line intervention when vocal fatigue is experienced by singer [20]. Stress and anxiety management is also crucial for maintaining the good psychological condition of a singer. The aim of physical and mental approach to prevention of vocal fatigue is optimisation of the performance efficacy [21]. This translate to minimising muscular activation, achievable by improving posture and relaxing muscles [22].

Professional opera singers often follow the vocal routine which usually begins under the influence of their singing teacher and speech-language pathologist. Vocal hygiene practices contain moderation in amount and type of voice use, reduction of stress, avoidance of phonotraumatic behaviours like shouting, talking over crowds, aspects like systemic hydration and humidification to improve performance and ensure voice longevity [23]. Effects of systemic hydration and vocal rest were proved to have a significant influence on the decrease of vocal fatigue and maintaining good vocal quality in general [16,24].

In literature, researchers postulated to set safety limits of vibration dose (phonatory time) for professional voice users to protect people in several occupations (singers, teachers). For instance, proper recovery time has been worked out for professional athletes who abuse their body in different ways. Importantly, Titze divided recovery for short- and long-term. The first one takes place immediately when phonation is stopped [25]. The primary benefit from short recovery is for the muscles whose chemicals get reset before next contractions. On the contrary, traumatised epithelial cells need more prolonged healing. Some of them after being heavily bombarded during vocal folds contraction can degenerate and be shed off. New cells will grow underneath, but that requires time. Furthermore, some destruction of the structural matrix of the lamina propria may be present after prolonged phonation. Fibroblasts activity is necessary for the repairing to continue constantly. The recovery process may range from several hours to 72h to complete [25]. As was presented in the study, the actual phonation for opera singers in 2–3h opera was of the series 20–30min for leading role, and their schedule performance was on the order of 3 per week [25]. Overall, these facts put opera singers in the favourable position for proper vocal recovery. Nevertheless, the type and loudness of phonation were not considered in research calculation, but they can play a tremendous role. Given this points, more research is needed to create appropriate guidelines to prevent singers from vocal fatigue.

Singers appear to be at particular risk of developing voice problems. Formal assessments of singers experiencing a voice problem at any given moment in a time range from about 20 to 50% [26]. Moreover, the impact of voice problems on quality of life was widely investigated in the literature. Many studies proved that decrease in voice quality and other voice impairments affects severely quality of life. Of course, in case of professional singers, this problem grows to the crucial role because directly concerns the source of income.

Attempts at analysing vocal fatigue in patients who already experienced this condition are difficult because of subject heterogeneity and burden with problems of data interpretation. Even individuals selected for having only symptoms of vocal fatigue usually present variable baseline and outcome data.

Professional opera singers have high stakes in sustaining excellent vocal condition but also experienced unique vocal demands, making them important population to study.

Useful tools to adapt to everyday practice are scales which help to evaluate singers’ perceptions of physical aspects of singing status. A good example is EASE scale (Evaluation of the Ability to Sing Easily) which is clinical outcome test for symptomatic aspects of compromised vocal health but was not designed as the primarily disease-specific instrument [27]. This test serves as the measure of potential changes in the singing voice which may indicate effects of vocal effort and may help to detect singers with the increased risk of possible development of voice disorders. The EASE was designed to help singers in assessing vocal load threshold, recovery time to assist performance scheduling, help to predict the development of vocal problems, evaluate therapeutic outcome in management for specific needs of the singer’s voice, lastly to provide supportive data for determining performance fitness [27].

Conclusion

Vocal fatigue may be underestimated but is one of the most frequent problems encountered in the ENT practice which provides care for professional voice users. The most frequent symptoms were muscle fatigue, diffuse sharp pain and muscle pain. In the study group, administration of anti-inflammatory drugs has not been associated with faster recovery from vocal fatigue.

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