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On-line version ISSN 2317-1782

CoDAS vol.30 no.1 São Paulo  2018  Epub Mar 05, 2018 

Original Article

Correlation between bulbar functionality and laryngeal penetration and/or laryngotracheal aspiration on motor neuron disease

Bárbara Carolina Brandão1  * 

Alline de Sousa Galdino1 

Luciano Garcia Lourenção2 

Glaucia Santana Trindade1 

Magali Aparecida Orate Menezes da Silva1 

Roberta Gonçalves da Silva3 

1Faculdade de Medicina de São José do Rio Preto – FAMERP - São José do Rio Preto (SP), Brazil.

2Universidade Federal do Rio Grande – FURG - Rio Grande (RS), Brazil.

3Universidade Estadual Paulista “Júlio de Mesquita Filho” – UNESP - Marília (SP), Brazil.



Describe and correlate bulbar functionality with laryngeal penetration and/or laryngotracheal aspiration for different food consistencies in Motor Neuron Disease (MND).


Study participants were 18 individuals diagnosed with MND regardless of the type and time of onset of disease. The Amyotrophic Lateral Sclerosis Functional Rating Scale - Revised/BR (ALSFRS-R/BR) was applied, and only the bulbar parameter, which includes speech, salivation and swallowing, was analyzed, with scores raging from 0 (disability) to 12 (normal functionality). Swallowing videofluoroscopy was performed using the Penetration-Aspiration Scale (PAS) described by Rosenbek et al. (1996). The Pearson correlation test was used for data analysis.


According to food consistency, the PAS level ranged from 1 to 5 for puree consistency, 1 to 4 for thickened liquid, and 1 to 3 for liquid, and no laryngotracheal aspiration was observed. Negative correlation between bulbar functionality and laryngeal penetration was observed for all food consistencies (pasty: r=-0.487, p=0.041; thickened liquid: r=-0.442, p=0.076; liquid r=0.460, p=0.073), but statistically significant difference was found only for the puree consistency, that is, individuals with poor bulbar functionality presented higher levels of laryngeal penetration.


Negative correlation was observed between bulbar functionality and laryngeal penetration in MND. The bulbar parameters of the ALSFRS-R/BR are significant for predicting risk of laryngotracheal aspiration for pasty consistency in MND.

Keywords  Motor Neuron Disease; Deglutition Disorders; Videofluoroscopy



Descrever e correlacionar a funcionalidade bulbar com penetração e aspiração laringotraqueal em distintas consistências de alimento na Doença do Neurônio Motor (DNM).


Participaram do estudo 18 indivíduos diagnosticados com DNM, independentemente do tipo e tempo da doença. Foi aplicada a escala Amyotrophic Lateral Sclerosis Functional Rating Scale–Revised/BR (ALSFRS-R/BR), sendo analisado apenas o parâmetro bulbar que compreende fala, salivação e deglutição, com pontuação de 0 (incapacidade) a 12 (funcionalidade normal). Realizou-se videofluoroscopia da deglutição com aplicação da Penetration-Aspiration Scale (PAS) descrita por Rosenbek et al. (1996). Realizado Teste de Correlação de Pearson.


Considerando a consistência do alimento, o nível da PAS variou de 1 a 5 na consistência pastosa, de 1 a 4 na líquida espessada e de 1 a 3 na líquida rala, e não houve aspiração laringotraqueal. Para todas as consistências de alimentos, houve correlação negativa entre funcionalidade bulbar e penetração laríngea (pastoso: r=-0,487, p=0,041; líquido espessado: r=-0,442, p=0,076; líquido ralo: r=-0,460, p=0,073), porém somente na consistência pastosa houve diferença estatística significante, ou seja, indivíduos com baixa funcionalidade bulbar apresentaram maior nível de penetração laríngea.


Houve correlação negativa entre funcionalidade bulbar e penetração laríngea na DNM. Os parâmetros bulbares da escala ALSFRS-R/BR mostraram-se significantes para predizer risco de penetração laringotraqueal na consistência pastosa na DNM.

Descritores Doença do Neurônio Motor; Transtornos de Deglutição; Videofluoroscopia


Motor Neuron Disease (MND) characterizes clinical syndromes in which involvement of the lower and/or upper motor neurons is observed, such as Amyotrophic Lateral Sclerosis (ALS), Progressive Muscular Atrophy (PMA), Primary Lateral Sclerosis (PLS), and Progressive Bulbar Palsy (PBP)(1,2).

These syndromes can cause dysphagia, and they affect up to 85% of individuals with ALS(3). Oropharyngeal dysphagia in this population is associated with progressive degeneration of the corticobulbar pathways to IX, X, XI and XII cranial nerve motor nuclei, causing secondary alterations in pharyngolaryngeal contraction and atrophy of the vagus and glossopharyngeal nerves, leading to difficulty in the palatine veil movement and decrease in laryngeal elevation, as they are responsible for the motor and sensory innervation of the larynx and pharynx(4). In addition, oropharyngeal dysphagia in this population is marked by changes in the oral phase of swallowing, which is justified by weakness, fasciculation, and tongue atrophy, thus determining oral incoordination with impairment to feeding(4).

Oropharyngeal dysphagia can occur regardless of the type of disease onset, either bulbar or spinal, with presence of laryngeal penetration and laryngotracheal aspiration in patients with MND(3-6).

There has been frequent search for MND progression indicators(7). Currently, there are scales that assist with monitoring the symptoms of these patients and providing specific parameters for each motor function.

Considering that, during evolution of MND, bulbar functions such as speech, salivation and swallowing, as well as motor function in general are impaired due to cranial nerve involvement, individuals with compromised bulbar function may present more severe dysphagia with presence of laryngeal penetration and laryngotracheal aspiration as the disease progresses. Identifying the moment at which individuals with MND present greater risk of laryngeal penetration and laryngotracheal aspiration can assist with the definition of therapeutic behaviors, as well as with the management of symptoms, avoiding nutritional and pulmonary complications and improving quality of life.

In view of the foregoing, the present study aimed to describe and correlate bulbar functionality with laryngeal penetration and laryngotracheal aspiration in patients with MND.


This study is part of the project “Association of Global Motor Performance with Oropharyngeal Dysphagia in Amyotrophic Lateral Sclerosis”, which was approved by the Research Ethics Committee of the Faculdade de Medicina de São José do Rio Preto (CAAE 53663516.0.3001.5415).

After receiving the necessary guidance and clarifications on the procedures to be conducted, all participants and/or caregivers signed an Informed Consent Form (ICF) prior to study commencement.

Study participants were 18 individuals (14 men and four women) aged 31-87 years (mean=55.66) diagnosed with Motor Neuron Disease (MND) by means of clinical examinations, regardless of the type and time of onset of disease. Of the individuals included in the study, 83.33% (N=15) were diagnosed with Amyotrophic Lateral Sclerosis (ALS), 11.11% (N=2) with Primary Lateral Sclerosis (PLS), and 5.55% (N=1) with Progressive Muscular Atrophy (PMA). Time of disease onset varied from six months to 10 years.

The Amyotrophic Lateral Sclerosis Functional Rating Scale – Revised/BR (ALSFRS-R/BR), translated and validated for Brazilian Portuguese(8), was applied to all participants and/or caregivers, in a private room, by a speech-language pathologist who read the options to the respondents, took notes of their answers, and posteriorly analyzed the results, ensuring the assessment standardization.

The ALSFRS-R/BR evaluates the bulbar function (speech, salivation, and swallowing), fine motor function (handwriting, cutting food and handling utensils, and dressing and hygiene), gross motor function (turning in bed and adjusting bed clothes, walking, and climbing stairs), and respiratory function (orthopnea and respiratory insufficiency) by scores ranging from zero to four for each item and a total score from zero (disability) up to a maximum score of 48 points (normal functionality). However, in this study, only items referring to the bulbar function (speech, salivation, and swallowing) were used, with scores ranging from zero (disability) to 12 (normal functionality).

Objective evaluation of swallowing was conducted by videofluoroscopy in the Radiology Department of the Hospital. The examinations were performed by a radiologist, a radiology technician, and a speech-language pathologist with experience in this procedure. The individuals remained seated and the images were taken in the lateral position with limits marked as follows: upper and lower, from the oral cavity to the esophagus; anterior, by the lips; posterior, by the wall of the pharynx; superior, by the nasopharynx; and inferior, by the cervical esophagus(9). A Flexavision-HB (Shimadzu Corporation) remote-controlled X-ray device coupled to a video converter was utilized.

The examination protocol began with the standardization of preparation of the consistencies. For puree consistency: 40 ml of water + 15 ml of barium sulfate (BaSO4) + 1 measure of food thickener; for thickened liquid consistency: 20 ml of water + 20 ml of barium sulfate (BaSO4). All consistencies were offered in a volume of 5 ml each, in a plastic spoon, with three 5 ml offers: first in puree consistency, followed by thickened liquid and thinned liquid; the supply was interrupted in the presence of laryngotracheal aspiration. In this study, the videofluoroscopy protocol used only the Penetration-Aspiration Scale (PAS)(10), which presents eight levels ranging from no laryngeal penetration (level 1) to presence of unresponsive aspiration from the patient, i.e., silent aspiration (level 8).

The correlation study between the bulbar parameters of the ALSFRS-R/BR and the levels of the PAS were performed individually for each food consistency, and the results were submitted to statistical analysis using the Pearson's correlation test, adopting a significance level of 95% (p≤0.05).


Table 1 shows the classification of individuals with Motor Neuron Disease (MND) according to the Penetration-Aspiration Scale (PAS) levels for each food consistency. No laryngotracheal aspiration was observed in any of the individuals in this sample.

Table 1 Classification by the Penetration-Aspiration Scale (PAS) of individuals with Motor Neuron Disease (MND) according to food consistency 

Individual Puree Thickened liquid Liquid
1 5 2 2
2 1 4 _
3 1 1 1
4 1 1 1
5 1 2 2
6 3 3 2
7 1 1 1
8 1 1 1
9 1 1 1
10 1 1 1
11 1 _ 1
12 2 2 -
13 1 1 1
14 1 1 1
15 1 1 1
16 2 2 3
17 1 1 3
18 1 3 3

ALSFRS-R/BR scores for the bulbar functionality are depicted in Figure 1. They range from one to 12, with fewer individuals near poor functionality or disability and more individuals close to normal functionality.

Figure 1 Distribution of individuals with MND in the Amyotrophic Lateral Sclerosis Functional Rating Scale - Revised/BR (ALSFRS-R/BR) for bulbar functionality 

Table 2 presents the correlation between bulbar functionality and laryngeal penetration for all food consistencies. Negative correlation was found for all food consistencies, but significant difference was observed only for the pasty consistency (p=0.041).

Table 2 Correlation between bulbar functionality and laryngeal penetration according to food consistency 

Bulbar functionality Laryngeal penetration Puree Laryngeal penetration Thickened liquid Laryngeal penetration Liquid
Absent Present Absent Present Absent Present
1 1 1 1
2 1 1
5 1 1 1 1 1 1
6 1 1 1
7 1 1 1
8 2 2 2
9 2 1 2 1 2 1
10 2 1 1 1
11 4 3 1 3 1
12 1 1 1
Pearson’s correlation test -0.487 -0.442 -0.460
p-value 0.041* 0.076 0.073

*Statistically significant

Figure 2 shows the individual distribution according to bulbar functionality and presence of laryngeal penetration.

Figure 2 Distribution of individuals with MND in the ALSFRS-R/BR by bulbar functionality and laryngeal penetration according to food consistency 


Motor Neuron Disease (MND) is strongly characterized by significantly compromising the overall and oropharyngeal motor controls, resulting in multiple damages to the general functional condition, as well as to the safety and efficiency of feeding in this population. Moreover, there are several risk factors to the quality of life of patients with MND, and the presence of oropharyngeal dysphagia is one of these risk markers.

According to the specific scientific literature, in addition to being a frequent comorbidity in MND, dysphagia affects the oral and pharyngeal phases, regardless of food consistency(11); however, patients with bulbar onset present impaired swallowing in the initial phase of the disease(12).

Presence of oropharyngeal dysphagia in the different underlying diseases, including the MNDs, may contribute to development of pulmonary complications and, therefore, presence of laryngeal penetration and laryngotracheal aspiration has become one of the most relevant parameters to be investigated in the context of clinical and objective assessment of this swallowing disorder. Nevertheless, although there are frequent reports in the literature on the presence of this symptom in MND(4,6), no individuals with laryngotracheal aspiration were found in the sample of this study. However, presence of laryngotracheal aspiration in MND is closely associated with the damage that this disease causes to the oropharyngeal functions and, at a certain moment, with its progression. Sometimes, depending on the type of MND, the oropharyngeal condition is severely compromised since the onset of disease, or it worsens with its progression. Furthermore, a study on MND showed that the presence of laryngotracheal aspiration in this population is related to the onset of bulbar symptoms for more than 24 months(12) and the sample of this study was heterogeneous from the bulbar point of view.

In contrast, different levels of laryngeal penetration were found in the individuals with MND for all food consistencies, evidencing presence of impairment in the oral and pharyngeal phases of swallowing. The different oropharyngeal pathophysiological mechanisms affected by MND begin with the presence of weakness in the tongue musculature, which causes difficulties in formation, containment, and propulsion of the food bolus, affecting pharyngeal response and triggering posterior oral leakage for all food consistencies, especially for liquids(12,13-15). Another common pathophysiological aspect in MND that contributes to presence of laryngeal penetration and risk of laryngotracheal aspiration is pharyngeal residue, determined by poor oral propulsion and weakness in pharyngeal contraction(16).

Negative correlation was observed between bulbar functionality and presence of laryngeal penetration for pasty consistency, that is, the poorer the bulbar functionality, the higher the level of laryngeal penetration. Other studies that evaluated functionality using the ALSFRS-R/BR or other functional scales have also evidenced this finding(4,17). This result suggests that the bulbar parameter of the ALSFRS-R/BR can be used as an instrument to suggest risk of laryngeal penetration in MND, corroborating the literature(12).

The bulbar parameters of the ALSFRS-R scale observed in patients with MND can assist with predicting risk of laryngeal penetration, aiding in the early diagnosis of oropharyngeal dysphagia.


The levels of laryngeal penetration, as well as bulbar functionality, in Motor Neuron Disease (MND) varied for all food consistencies in the study population. In addition, negative correlation was observed for pasty consistency - the poorer the bulbar functionality in MND, the higher the level of laryngeal penetration.

Study carried out at the Hospital de Base, São José do Rio Preto, SP, Brazil.

Financial support: nothing to declare.


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Received: March 20, 2017; Accepted: August 19, 2017

Conflict of interests: nothing to declare.

*Correspondence address: Bárbara Carolina Brandão Faculdade de Medicina de São José do Rio Preto – FAMERP Av. Brigadeiro Faria Lima, nº 5416, Vila São Pedro, São José do Rio Preto (SP), Brazil, CEP: 15090-000. E-mail:

Author contributions BCB and ASG collected, classified, analyzed, and interpreted the data and assisted with the writing of the manuscript; LGL, GST, and MAOMS participated in the writing of the manuscript and critical review of relevant intellectual content; RGS was responsible for the study design, collection, analysis, and interpretation of the data, and writing of the manuscript.

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