Correlation of the Maximal Respiratory Pressures, Respiratory Airflow and Dysphagia in Patients with Acquired Autoimmune Myasthenia Gravis

Research Article

Austin J Musculoskelet Disord. 2016; 3(1): 1031.

Correlation of the Maximal Respiratory Pressures, Respiratory Airflow and Dysphagia in Patients with Acquired Autoimmune Myasthenia Gravis

Oda AL¹*, Bolzan DW², Cruz CTV³, Oliveira ASB4 and Raimundo RD5

¹Neuromuscular Discipline, Federal University of São Paulo, Brazil

²Cardiology Discipline, Federal University of São Paulo, Brazil

³Faculdades Metropolitanas Unidas, Brazil

4Neuromuscular Discipline, Federal University of São Paulo, Brazil

5Faculdade de Medicina do ABC e Faculdade de Saúde Pública da Universidade de São Paulo, Brazil

*Corresponding author: Oda AL, Neuromuscular Discipline, Federal University of São Paulo, Brazil

Received: May 15, 2016; Accepted: June 03, 2016; Published: June 06, 2016


Introduction: Patients with Acquired Autoimmune Myasthenia Gravis (AAMG) have a frequent complaint of muscle fatigue, resulting in respiratory distress, associated or not to the signs and symptoms of dysphagia.

Objective: to characterize the measures of respiratory and appendicular muscle strength, expiratory and cough peak flow and relate to the degree of dysphagia in patients with AAMG.

Methods: We assessed 20 patients with a diagnosis of Acquired autoimmune myasthenia gravis, being 14 (70%) female and 6 (30%) male, with an average age of 38.71 and 50.16 years, respectively. The following procedures were performed: speech and swallowing evaluation and respiratory clinical evaluation. It was incorporated measures of maximum inspiratory pressure, maximum expiratory pressure, peak expiratory flow and peak cough flow.

Results: there was a statistically significant relationship between alteration of muscles of lips, tongue and buccinator and the severity of dysphagia. 70% of patients referred to dyspnoea, being that the averages of percentage of predicted of MEP and MIP, PFE were below 80% in patients with dysphagia. Significance was found in the correlation between measures of force and of respiratory airflow.

Conclusion: the strength of cough expiratory flow is correlated to the inspiratory and expiratory muscle force. The involvement of the orofacial musculature and reduced values of MIP, MEP and PFE were indicators of the deterioration of oropharyngeal dysphagia. Both measures of respiratory muscle strength are lower than predicted.

Keywords: Neuromuscular diseases; Myasthenia gravis; Deglutition; Deglutition disorders; Respiration; Muscle strength


AAMG: Acquired Autoimmune Myasthenia Gravis; l/min: Liters/Minute; mg: Milligram; MIP: Maximal Inspiratory Pressure; MEP: Maximal Expiratory Pressure; PCF: Peak Cough Flow; PEF: Peak Expiratory Flow


Neuromuscular diseases are a group of disorders that compromise the motor unit (i.e. the lower motor neuron of the cell body, its extension, the neuromuscular junction or muscular tissue [1-3] without cardiovascular, hormonal or metabolic implications [3]. Among the neuromuscular diseases that usually affect the stomatognathic system functions (breath, voice, speech, chew and swallow), the Myasthenia Gravis has a special importance [4].

The most frequent symptoms are strabismus, diplopia, ptosis, dysphagia, dysarthria, dysphonia, dyspnea and fatigue. Fatigue symptoms seem to be worse in the afternoon period and can be aggravated by physical exercise, infections and emotional factors. The most affected muscle groups are the oculomotor, orbicularis oculi muscles, masticatory and those dependent of the ninth and tenth cranial nerves [5].

Dysphagia may be the first or the only symptom of disease [6]. Bulbar alteration may be the only manifestation of Myasthenia Gravis, and the patients may have nasality changes, nasal reflux, and difficulty in food bolus control with possible bronchoaspiration [7].

The impairment of respiratory muscles is unsystematic, varying from dyspnea at rest until intense dyspnea on exertion [4]. The worsening of respiratory function can be related to the myasthenic crisis, where the patient presents a severe weakness compromising the proper airway functioning [8].

Characteristic muscle weakness of AAMG leads the patients to present respiratory disorders (i.e. dyspnea and respiratory accessory muscles use), and to monitor respiratory function, especially during daily living activities. For this reason the constant decline of the vital capacity, inspiratory muscles pressure, and loss of the upper airway integrity are commonly observed [9]. The impairment of respiratory function may involve, dysphagia worse, explained by pressure changes in laryngeal structures. Therefore, myoelastic component alteration (by weakness and muscle fatigue) add to the aerodynamic component change (by pressure reduction in the airways) could influence a more severe dysphagia scenario. Oropharyngeal dysphagia is a highly debilitating condition and should be evaluated and treated in the course of the disease avoiding secondary complications (i.e. nutritional deficiency, dehydration and pulmonary complications due to tracheal aspiration) [4].

The aim of this study was to evaluate and characterize the respiratory and peripheral muscles strength, expiratory peak flow, and peak cough flow, and establish a possible correlation of these variables to the dysphagia degree in these patients with AAMG.5.

Materials and Methods

This study was conducted at outpatient research sector in neuromuscular diseases of the Federal University of São Paulo, Brazil. The local institutional ethics committee approved this study. All patients were informed, and written consent was given prior to inclusion.


A total of 20 patients of both genders, with diagnosis of ocular, bulbar or generalized forms of acquired autoimmune myasthenia Gravis were prospectively included.

Congenital Myasthenia Gravis or other diagnoses served as our primary exclusion criteria. Patients with acute or chronic respiratory diseases, smokers and age below 18 years old were also excluded.

Patients underwent a respiratory evaluation with data MIP, MEP, PEF and PCF. In addition, a clinical assessment was carried out, with emphasis on chewing and swallowing functions, according to the protocol used in Neuromuscular Disease Research Sector UNIFESP38.

Study design

The general patient data were obtained from the medical file of the aforementioned Research Sector in Neuromuscular Diseases.

All patients were submitted to an initial clinical assessment. The anatomical and functional aspects of the neck, face and speech organs were evaluated by the observation of the posture configuration, mobility, tension and force in rest, spontaneous and guided movement. Muscle groups of lips, tongue, buccinator, masticatory and soft palate were evaluated.

Patients were also submitted to a respiratory evaluation. In addition, a clinical assessment was carried out, with emphasis on chewing and swallowing functions, according to the protocol used in Neuromuscular Disease Research Sector of the Federal University of São Paulo [10].

Chewing function evaluation

We observed the lips posture, strength, amplitude, speed and direction of movement; cut and food lateralization; associated movements and masticatory efficiency. Moldy french bread was used for evaluation, due to the proper consistency to the observation of the aforementioned items.

Swallowing function evaluation

Swallowing was evaluated in relation to the process efficiency, and the following criteria was observed: sealing lip; posture, mobility and driving force of the tongue; containment of the food bolus in the oral cavity; associated movements; waste accumulation in the oral cavity; laryngeal elevation; nasal reflux; presence of coughing during or after swallowing; “wet” voice after swallowing, and coordination swallowing and breathing. In addition to the complaint referred to the stasis in laryngeal-pharyngeal and esophageal region were evaluated. Swallowing was evaluated in four distinct stages:

• Saliva: patients was observed in situations of rest, spontaneous and directed movement; in relation to saliva accumulation in oral vestibule and/or corners of the mouth, previous leak of saliva and presence of cough or choke with their own saliva.

• Thickened liquid: by administration of water in measures of 1, 3, 5 and 10 ml, offered in a disposable cup and spoon.

• Paste: by administration of natural yogurt (consistent type), in measures of 1, 3, 5 and 10 ml, offered to the patient in a disposable spoon.

• Solid: by administration of Moldy french bread.

After the aforementioned evaluation, the findings were classified as normal (0), mild (1), moderate (2), severe (3), and deep (4) according to the criteria proposed by Chiappetta and Oda. The severity classification table includes areas of evaluation focused on the oral (oral contention of food/saliva, trituration, lateralization, accommodation and ejection food bolus, and the presence of residues in the oral cavity), pharyngeal phase (laryngeal elevation, nasal reflux, residues in pharyngeal recess, laryngeal penetration, tracheal aspiration) and esophageal phase (decrease of rhythm and peristaltic contraction force).

Respiratory evaluation

For respiratory assessment, we measured the maximum inspiratory pressure; maximum expiratory pressure, peak expiratory flow and peak cough flow.

In the present study, the tests were performed with facial mask to avoid bias and minimize the possible air leak around the nozzle secondary to the mouth orbicularis muscles weakness.

A manovacuometer (Gerar®) graduated in cm H2O (0-155), were used to evaluate the Maximum Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP). The measures were performed at Functional Residual Capacity (FRC) with the patients confortable sitting. The tests were performed according to the standards of the American Thoracic Society (ATS) [12]. The predicted values were calculated according to a previously described equation [13].

To Peak Expiratory Flow (PEF) and Peak Cough Flow (PCF) evaluation, we used a peak flow meter (Mini-Wright Airmed®) graduated in L/min (60-850). This equipment was coupled to a mask without exhalation valve. Patients were instructed to maintain the sitting position and perform a maximal inspiration effort until to total lung capacity and perform a strong and fast expiration, with maximum expiratory effort possible, keeping the lips open to avoid resistance to the air flow (PEF), and with a strong and unique cough (PCF) through the mask.

The maneuvers (PFE and PCF) were repeated three times and the highest measure value was selected for analysis. If the last measure was the largest value, the procedure was repeated up to a maximum of five times.

In all cases, to avoid air leak, the examiner helped the patient in relation to the mask positioning and fixing. Measures with air leak were discarded. Patients were instructed to avoid trunk flexion or neck, as well compensatory movements during the procedure.

Statistical analysis

Continuous data were described as mean and standard deviation, and compared by Analysis of Variance for Not Repeated Measures with Gabriel’s post-test. Continuous data of different variables were correlated using Pearson correlation test and the degree of linearity (r) and significance (p) were evaluated.

Categorical data were represented by absolute frequency (n) and relative (%) and compared using Pearson’s chi-square test. For all study alpha risk <5% was considered.


This study evaluated 20 patients. Demographic data related to sex, age, referred disease and diagnostic time are described in (Tables 1 and 2).