Application of subjective and objective tools for the evaluation of the articulatory organs among patients with amyotrophic lateral sclerosis

Amyotrophic lateral sclerosis (ALS) is a fatal degenerative disease of a rapid course. In 25% of ALS sufferers, speech disorders occur as prodromal symptoms of the disease. Impaired communication affects physical health and has a negative impact on mental and emotional condition. In this study, we assessed which domains of speech are particularly affected in ALS. Subsequently, we estimated possible correlations between the ALS patients’ subjective perception of their speech quality and an objective assessment of the speech organs carried out by an expert. The study group consisted of ALS. The patients were examined for articulatory functions by of Voice Handicap Index (VHI) and the Frenchay Dysarthria Assessment (FDA).


Introduction
Amyotrophic lateral sclerosis (ALS) is a rapidly progressing and ultimately fatal neurological disease characterized by gradual degeneration of the upper and lower motor neurons. Bulbar dysarthria, which is the commonest form of speech impairment in ALS (exhibited by 80 % of the sufferers), accelerates the progression of the disease and contributes to a considerable decline in quality of life [1][2]. In 25 % of ALS patients speech deterioration is the first symptom of the disease [3]. A reliable diagnosis of ALS is a lengthy process mainly based on clinical observation, which is why an accurate diagnosis is often delayed, even by 12 months [4].
Despite having little impact on physical health, impaired communication adversely affects mental and emotional wellbeing [5]. Of all the articulatory organs the tongue is where the debilitating effects of ALS can be observed first. As the disease progresses it affects the perioral area and the jaw [6][7][8]. Compared to healthy individuals, ALS sufferers while speaking demonstrate slower and prolonged jaw and lips movements [5][6][7][8]. It has also been established that the data obtained from the observation and analysis of the articulators efficiency can be utilized as a practical clinical marker for a reliable assessment of ALS progression and the extent of speech deterioration [9]. ALS individuals present a 30% reduction of the tongue mass and a decline in the mobility of the lower lip and jaw. These changes have a more severe adverse effect on speech intelligibility than a functionally debilitating defect of any other component of the articulatory system [9][10].
The speed of ALS progression is measured by means of various clinimetric scales. The most commonly used global assessment instruments comprise: the ALS Functional Rating Scale-Revised (ALSFRS-R), the Norris Scale, Appel the ALS Rating Scale or the ALS Severity Scale [11]. For the quantitative evaluation of the efficiency of the articulatory organs, Frenchay Dysarthria Assessment (FDA) is the most frequently recommended scale [12][13]. Whereas, speech intelligibility can be measured using the Computerized Assessment of Intelligibility of Dysarthric Speech -Sentence Subtest [14]. The main objective of this software ismonitoring the progression of speech impairment in patients staying at home. The system is endowed with a feature enabling to control speech quality during their telephone conversations with the therapist. This, however, is not recommended as a reliable clinical measure for the evaluation of speech deterioration in ALS [15]. An alternative tool used for the objective assessment of ALS progression is the Multi-Dimensional Voice Program, based on a multi-parameter acoustic analysis [16].
Relevant research and reliable tests allowing a quick assessment of speech quality by the patients themselves are still scarce. Existing studies indicate that such an assessment is possible but would require sophisticated software or instruments, which might be too costly for the patients or their families [12].
Voice Handicap Index (VHI) is an unsophisticated and convenient tool for the assessment of speech impairment which can be applied by ALS patients themselves in their home environment [17]. Owing to this instrument people with ALS can subjectively evaluate the impact their deteriorating speech has on their subjective perception of a decline in quality of life. The index is made up of 3 components, each dedicated to a different aspect: functional, physical and emotional. The functional subscale measures the extent of the influence of voice deterioration on the subject's everyday functioning; the physical one allows the assessment of the articulatory organs efficiency, whereas the emotional component enables to monitor the subject's emotional reaction to the progressive speech deterioration [18][19]. VHI is a valid and reliable instrument approved by the Agency of Healthcare Research and Quality in 2002 [20].
The first goal of this study was to assess which domains of speech are particularly involved in ALS patients. The second aim of the investigation was to estimate possible correlations between subjective sense of speech disturbances experienced and self- The study enrolled 63 patients -25 females and 38 males-aged between 27 and 65 years old (mean: 57.03 ± 15.75) with sporadic ALS [21] according to the El Escorial Revised Criteria [22]. The exclusion criteria involved individuals suffering from any concomitant conditions affecting speech quality as well as those aged over 65 years due to the agerelated decline in speech [23].

Speech test-VHI questionnaire
International research projects have demonstrated that the VHI questionnaire is a reliable tool for the subjective evaluation of voice in ALS patients and that the scores it provides are consistent. The 30-item VHI questionnaire, which comprises 3 subscales of 10 items each: the physical (P) items, functional (F) items and emotional (E) items, is a recommended method of subjective assessment of the severity of speech disorders by ALS patients themselves. Cronbach's alpha for the entire cohort was 0.95, indicating high internal consistency of the 30 items. The VHI is a reliable and valid diagnostic tool that can be recommended for ALS individuals. The questionnaire is widely used throughout the world in a number of language versions including Persian, Croatian, Italian, Brazil, Latvian, Greek, Polish and many others [24][25][26][27][28][29][30]. Based on a detailed analysis of the VHI scores the patients were divided into group I with slight speech quality disorders (0-30 score range) and group II with medium and deep disturbances in the quality of speech (31-120 score range). Such a division allowed us to compare the differences between mild, medium and deep disturbances in the quality of speech in adequately large groups.

Speech test-FDA
One of the most important objective tests for evaluating the articulatory organs is the Frenchay Dysarthria Assessment (FDA). The FDA is a standardized test which relies on a 9point rating scale applied to a patient. It provides information based on the observation of oral structures, functions and speech. The test evaluates the following functions: reflexes, respiration, tongue, lips, the soft palate, larynx, intelligibility. A 5-point rating scale (a-e) is used for the assessment, where letter 'a' represents norm, 'b' mild severity, 'c' moderate severity, 'd' considerable severity, 'e' profound severity. FDA is also used to assess the severity of the articulatory organs disorders and to monitor the effects of the treatment [13]. The test was conducted by a clinical speech therapist with 12 years' experience of treating neurological conditions, predominantly Parkinson's disease (PD).
The second edition of FDA utilizes the latest findings concerning motor speech disorders and their contribution to a neurological diagnosis. It has good feasibility (missing data <5 %), a high reliability of the total score (0.94), an excellent inter-rater agreement for the total score (0.96) and moderate to large construct validity for 81% of its items [13,30].

Statistical analysis
The first goal of the study was to assess which domains of speech are particularly involved in ALS patients. The second aim of the investigations was to estimate possible correlations between a subjective sense of speech disturbances experienced by ALS patients and an objective assessment performed by an expert. The null hypotheses were that (1)  Results 63 patients participated in the study and were evaluated using the FDA and VHI scale.
After analyzing the results, the patients were divided into two groups depending on the obtained VHI score. Group I consisted of 40 patients with slight speech quality disorders (0-30 points), and group II consisted of 23 patients with mean and profound speech quality disorders (31-120 points). Table 1 presents the general characteristics of the studied population of ALS patients. Table 2 illustrates the correlation between age, sex and duration of the disease within particular groups according to VHI scale. No significant differences between selected parameters were found. Table 3 illustrates the exacerbation of articulatory disorders in patients constituting groups I and II, measured by objective means of FDA. In group I subjects, the efficiency of the articulators was within normal limits or mildly impaired, whereas in their counterparts from group II the impairment was of moderate to severe degree. Table 4

Discussion
Speech disorders are one of the most common manifestations of ALS and a real challenge for both clinicians and researchers [31]. Early dysarthric symptoms occur sporadically and usually come in the form of hoarseness and declined speech at the end of the day. As the disease progresses, the symptoms become more severe -the muscles of the tongue, lips and larynx get weaker and slower, their movement amplitude decreases and speech intelligibility declines [32].
Some researchers argued that speech impairment in ALS is more prevalent in females [33]. Our study did not confirm the finding. Quite the opposite, even though the difference was statistically insignificant, we found that it was the male subjects who were affected by speech deficits more often (60.31%) than women. This could result from the fact that ALS incidence rates are higher among men [2].
Tongue dysfunction is commonly considered as one of the typical symptoms of speech deterioration in an early stage of ALS [5,34]. Other symptoms include a decline in the functionality of the soft palate, larynx and lips [34][35].
Among the participants of our study who presented mild speech impairment established by means of the FDA scale, the most prevalent abnormalities were observed in tongue mobility (63.2%), soft palate (70%) and lips (72.5%). The obtained results correspond with the current state of knowledge on the subject [34][35].
The main measure of communication efficiency in ALS subjects is the extent to which their speech is comprehensible. Impaired speech undoubtedly affects quality of life and the severity of communication deficit is a determinant of the treatment option that ought to be applied [10]. Speech intelligibility could be treated as a practical measure used in monitoring the quality of articulation during the course of treatment as well as the assessment of the progression of the disease process [36].
Yunusova et al. demonstrated the existence of a direct relationship between speech intelligibility and the mobility of the lips and jaw in ALS subjects [34]. Other researchers reported lack of correlation between speech comprehension in ALS and progression of the disease [37]. It has also been found that in the early stages of the disease the reduced Our study shows that the ALS patients presenting mild impairment of the articulatory system, measured using the objective FDA scale, do not perceive significant deterioration of speech intelligibility, established by means of the subjective VHI. It is not until the occurrence of a considerable decrease in the articulators efficiency that a substantial decline in speech becomes evident. We found that a speech intelligibility decline coincides with dysfunctions in the length of phonation, pitch and voice volume. Also, the study revealed the existence of a correlation between FDA-based assessment of speech deterioration and the patient's perception of a decline in the physical and functional aspects of everyday life established by means of the VHI. These findings provide a valuable contribution to the knowledge of ALS progression and its impact on life quality of ALS sufferers.
Existing research does not mention any relationship between a progressive deterioration of motor functions and disorders of emotional nature [40]. Some earlier publications noted 'the disability paradox' phenomenon, a term that refers to the alleged lack of relationship between the subjective perception of physical dysfunction reported by ALS patients and a decline in quality of life [41][42]. Others, on the other hand, pointed to a weak or moderate correlation between the disease severity and the emotional condition of the sufferer [43]. The latter pattern was reflected in our study-the participants complained of a depressed mood they experienced in line with the progression of speech deficits.
The progression of speech deterioration in ALS is very rapid, which is reflected by the fact that the median survival for the disease is merely 30 months [44]. It is therefore vital that the process of speech deterioration should be monitored in a clinical setting so that new communication strategies could be devised and introduced in time. However, the range and reliability of currently available instruments for adequate monitoring of the articulatory functions is still insufficient. The limitations mainly concern the number of factors affecting the accuracy of the relevant examinations, their validity and reproducibility. Normalized diagnostic procedures applied for the evaluation of articulation quality and monitoring speech regression in ALS are very scarce [37]. This can be attributed to the logistic difficulty connected with the analysis of bulbar symptoms.
Shortages of proper tools for the assessment and monitoring of speech deterioration are commonplace in clinical environment. The procedures in most instances require the employment of sophisticated instruments such as tensometric sensors or air pressure bulbs, whose reliability and precision are yet to be properly documented [37,45]. One of the earliest predictors of ALS progression is a decline in the movement velocity of the articulatory organs [37].
The tools that we applied in our study to monitor the efficiency of the articulators and speech intelligibility comprised the FDA and the VHI rating scales. We demonstrated the existence of a high, positive correlation between the scores obtained from the two measures. The extent of a decline in the performance of the articulatory organs established by an experienced researcher corresponded with the patient-reported selfassessment of speech comprehensibility. These findings were substantially different from the outcomes of another study we carried out on the subjective and objective assessment of the extent of articulatory disorders in PD patients [30]. It may be the case that Parkinsonian patients are well-adjusted to the changes in the articulatory system. It needs to be noted that the average duration of Parkinson's disease is 15.8 years [46] compared to 30 months in the case of ALS [47]. Consequently, a dramatic speech deterioration in ALS is observed within a significantly shorter space of time. The results of this study imply that the VHI could be used as a reliable self-applied instrument for monitoring the course and progression of speech impairment in ALS as well as a prognostic instrument for predicting the progression of speech deterioration, which apart from being an early marker of acute speech exacerbation [37], is of critical importance in the context of therapeutic procedures for ALS. In the light of the abovementioned facts, it can be assumed that the VHI is a reliable marker of speech decline in ALS and thereby a useful tool for the verification of the onset of the symptoms and their progression, which will ultimately help to introduce proper therapeutic strategies.

Final remarks
The pathologic changes that occur in the tongue, lips and soft palate are typical features of the early symptoms of ALS. Individuals with ALS reported perceived speech decline at the time of the onset of phonatory impairment. A decline in the efficiency of the articulatory organs adversely affected social, physical and emotional functioning. A strong positive correlation was found between an objective evaluation of the articulators' efficiency performed by a specialist using the FDA scale and a subjective self-assessment of the feature conducted by the patients utilizing the VHI scale. It can be concluded that the VHI constitutes a valid measure of the articulation disorders in ALS patients, contributing to the decision making process regarding the compensatory treatment options aimed at the articulators affected by the disease.