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Introduction

Swallowing is a neuromuscular complex act that requires strict neurophysiological and sensorial and motor component control. It comprises two voluntary phases (preparation and oral) and two involuntary phases (pharyngeal and esophageal). The causes of swallowing disorders are varied and the approach of dysphagic patients should be multi-disciplinary. The otorhinolaryngologist has become increasingly involved in diagnosis and treatment of patients with dysphagia 15.

Swallowing disorders in children have been little studied, especially concerning the pharyngeal phase. Nevertheless, they may lead to malnutrition and recurrent pulmonary infections, if tracheal aspiration of the oropharyngeal content is experienced. A number of diagnostic methods are used, such as oral cavity ultrasound, surface electromyography, pharyngoesophageal manometry, pulmonary scintigraphy, swallowing videofluoroscopy and, recently, nasoendoscopic assessment.

Langmore, Shatz and Olsen (1988) defined fiberoptic endoscopic or nasoendoscopic assessment in swallowing using the method to investigate patients with difficulties or incapacity to perform videofluoroscopy.

Bastian (1993), Langmore and McCulloch (1997) described the method, indications, contraindications and risks, together with abnormal findings of the fiberoptic examination of swallowing.

It is a safe and widely used method by otorhinolaryngologists, providing structural information on the region of the airways and upper digestive tract. By making some modifications to the original procedure and administering food with contrast, the pharyngeal phase of swallowing may be objective studied, enabling functional assessment of swallowing in the pharyngolaryngeal phase.

The purpose of the present study was to use nasoendoscopy examination to investigate swallowing pharyngeal phase in a specific group of children, characterizing the applicability of the method and the observed alterations, especially concerning tracheal aspiration.

Material and Method

Material

We evaluated 218 children with cerebral palsy and complaint of dysphagia between March 1998 and March 2000, participants of the rehabilitation program of AACD - Associação de Assistência à Criança Defeituosa (Association for Care of Handicapped Children). Clinical diagnosis and classification of motor impairment of children with cerebral palsy were previously made by the medical team of the institution, using Hagberg's classification7.

In cases suspected of oropharyngeal dysphagia, children were initially assessed at the Clinic of Dysphagia at AACD by speech therapy specialized professionals and next referred to the ENT examination.

Method

In 134 of the 218 patients, ENT examination was complemented with swallowing functional fiberoptic endoscopic assessment, according to the protocol suggested by Langmore et al. (1988), followed by modifications proposed by a previous study.

We experienced some difficulties to comply with the protocol due to motor and cognitive impairments of some of the studied children. As a result, some modifications were necessary to reach satisfactory results; we omitted all tasks that required the patient's participation and administered smaller volumes (up to 5ml) since they were all children. In addition, since the children could not manipulate solid foods because of motor restrictions, we evaluated only liquid and paste foods.
Children were evaluated in the ambulatory, on a seated position and restrained by the accompanying person to prevent spontaneous or involuntary reflexes that could interfere in the test.

Foods were dyed with aniline (blue or green) and were administered by an assistant, using a graduate 10ml syringe. Fruit juice was employed to analyze liquid consistency (liquid contrast) and yogurt for paste consistency (paste contrast).

We administered increasing volumes of 1, 3 and 5ml of contrast, first paste and then liquid.

We used nasofiberscope Olympus 5 mm diameter, which has upper and lower deflection and aspiration channel, and in smaller children we used the flexible nasoendoscope Olympus ENF typo P3 of 3.2 mm. The camera used was Toshiba, videocassette Toshiba, color monitor Sony and videocassette JVC-SX 120.
The fiberoptic endoscope was introduced preferably through the left nasal fossa, progressing into the floor, according to the protocol previously defined for the Ambulatory of Dysphagia, Discipline of Otorhinolaryngology, UNIFESP/EPM. We did not apply anesthetics or topical vasoconstrictors.

Initially we performed structural and functional assessment, without food, observing nasal cavity, rhinopharynx and velopharyngeal sphincter during spontaneous saliva swallowing. By lower deflection of the device, we could observe the base of tongue, vallecule, lateral and posterior pharyngeal walls, pyriform recesses and the larynx, as well as salivary stases on the structures.

Mobility and movement of vocal folds were observed during crying and/or saliva spontaneous swallowing, or during speech, if the patient had phonation skills or could respond to simple questions. Next, we administered food contrast by oral route, through a 10ml syringe.

Tests were recorded in video and later the following findings were analyzed:

1. Early leak of the contrast into the larynx and/or pyriform recesses, characterized by the presence of food in the hypopharynx or larynx before the swallowing reflex had been triggered, which is identified at the fiberoptic examination as an epiglottic retroversion 10;

2. Laryngeal penetration characterized by presence of contrast in the laryngeal vestibule, comprising epiglottic laryngeal space, aryepiglottic folds, interarytenoid region, vestibular folds and ventricles, up to the superior face of the vocal folds10;

3. Tracheal aspiration, characterized by contrast flow on the region situated below the vocal folds, subglottic region and trachea, any time during swallowing10;

4. Presence of remains of food after swallowing, characterized by accumulation of contrast after the third swallowing, on the tongue base, vallecule, pyriform recess and posterior laryngeal wall1;
5. Presence of effective cough, characterized by the capacity to eliminate the contrast from the larynx after laryngeal penetration and/or tracheal aspiration1;

6. Assessment of laryngeal and pharyngeal sensitivity, characterized by responses of nausea or cough depending on the stimulated region10.

STATISTICAL ANALYSIS

We reported data in both absolute and percentage formats and data concerning the presence of early leak and tracheal aspiration of contrasted foods were statistically analyzed in order to try to define significant correlation among them. The test we used was kappa coefficient of Cohen (agreement measure).

Results

The 218 studied children had clinical diagnosis of cerebral palsy, and 120 (55.0%) had tetraplegic spastic type; 52 (23.8%) had diplegic spastic type; 11 (5.0%) had chorea-athetosis diskinesic type, and 35 (16.0%) had other clinical types.

Ages varied from 4 months to 14 years, mean age of 5.3 years, and there were 126 male children (57.8%) and 92 female children (42.2%).

Structural and functional alterations observed without food were: pharyngeal tonsil hypertrophy in 94 cases (43.1%); palatine and pharyngeal tonsil hypertrophy in 46 cases (21.1%); velopharyngeal insufficiency in 16 cases (7.3%); salivary stasis in 21 cases (9.7%); vocal folds paralysis in 9 cases (4.1%); presence of tracheostomy in 10 cases (4.6%).

As to swallowing assessment, 134 (61.5%) were evaluated through fiberoptic endoscopic examination, whose findings are presented in Tables 1 to 9.

In our study, no children presented complications or any events during the examinations, nor infectious complications resultant from aspiration.

Table 1.

Table 2.

Table 3.

Table 4.

Table 5.

Table 6.

Table 7.

Table 8.

Table 9.

Discussion

There are few published data describing the characteristics of swallowing difficulties in children, especially in neurologically affected patients, such as children with cerebral palsy. We believe that assessment of oral and pharyngeal swallowing phases are essential to characterize dysphagia in such children and to guide eating habits.

Cerebral palsy is a term used to designate a group of motor and non-progressive persistent abnormalities, which are not necessarily unchangeable, resulting from nervous system damage on the first stages of development20. It affects 2 in 1,000 living births in the United States4.

The swallowing phases most critically affected in children with cerebral palsy are pre-oral and oral phases, as a result of the damage to the cortical-bulbar and cortical-spinal tracts that affect the voluntary or cortical component of swallowing4. However, we tried to observe the pharyngeal phase and characterize the alterations through fiberoptic endoscope assessment, because the few studies published with cerebral palsy children have emphasized that pharyngeal phase abnormalities and aspirations are frequent. Manrique (1998) summed up the causes of dysphagia in children with cerebral palsy, emphasizing lack of coordination of swallowing and ventilation, oral motor abnormalities, delay in firing of swallowing reflex and compromised cognitive level.

Most studies investigating swallowing employed clinical assessment and videofluoroscopy. However, there are usually a number of patients who require structural and functional assessment of the larynx and pharynx; in addition, there are circumstances in which a videofluoroscopy can not be performed, such as in clinically unstable patients in the ICU; patients that can not be properly positioned for videofluoroscopy, patients who are clinically impaired and do not tolerate even small amounts of tracheal aspiration during the exam, and patients who have to be immediately assessed. Based on these needs and using flexible endoscope routinely in the ambulatory, the use of nasoendoscopy has been advocated for the functional assessment of swallowing.

According to Manrique (1998), complications and risks of nasoendoscopy are: nasal bleeding, mucosal damage, nausea and/or vomiting, side effect of the use of topical vasoconstrictor and topical anesthetics, laryngospasm and vagal reaction.

In the present study we evaluated 126 boys (57.8%) and 92 girls (42.2%), mean age of 5.3 years.

Structural and functional alterations observed were: pharyngeal tonsil hypertrophy in 94 cases (43.1%); palatine and pharyngeal tonsil hypertrophy in 46 cases (21.1%); velopharyngeal insufficiency in 16 cases (7.3%); salivary stasis in 21 cases (9.7%); vocal folds paralysis in 9 cases (4.1%); presence of tracheostomy in 10 cases (4.6%). However, we believe that these abnormalities were not the only cause for pharyngeal phase compromise and aspiration pathogenesis, but rather aggravating factors, since they can modify ventilation rest, preventing the children from coordinating swallowing and ventilation.

We observed during the fiberoptic endoscopic functional swallowing assessment the following aspects: early contrast leak into the pharynx (53.7%), laryngeal penetration of paste food contrast (4.8%), laryngeal penetration of liquid food contrast (5.2%), tracheal aspiration of paste food contrast (14.9%), tracheal aspiration of liquid food contrast (33.6%), remains of the contrast after swallowing (7.5%), efficacy of cough to eliminate the contrast from the airways (43.3%), and presence of laryngeal sensitivity (87.3%).

Early leak of the bolus into the pharynx was the most frequent alteration, observed in 72 children (53.7%), similarly to the data reported by Langmore (1988). In a comparative study, Wilson (1992) observed delayed triggering of reflex in 46.6% of the dysphagic patients and in none of the normal subjects.

In our assessment, there were statistically significant differences between early leak of food contrast and presence of tracheal aspiration of liquid and/or paste contrast. Helfrich-Miller (1986) reported that the higher it takes to fire the swallowing reflex, the higher the likelihood of aspirating the food bolus, because the tract remains opened up to the moment the swallowing reflex is fired. We believe that early leak of bolus into the pharynx is related to tracheal aspiration before swallowing, when the tract is left unprotected. In the present study, we did not characterize aspiration towards swallowing, but we do think that such correlation is important to help us define the cause of tracheal aspiration.

In our study, we did not observe absence of swallowing reflex firing, but there was delay in firing, despite the fact that the studied children had severe neurological impairments.

We noticed that there was laryngeal penetration of paste food contrast in 6 children (4.8%) and liquid contrast in seven cases (5.2%).

Tracheal aspiration of paste contrast was observed in 20 children (14.9%) and aspiration of liquid contrast in 45 (33.6%). Gisel and Benson (1996) reported a rate of 60% of aspiration of liquids in severely impaired cerebral palsy children , and 26% in moderately impaired children, through videofluoroscopy. Rogers (1994) found 38% of aspiration in videofluoroscopy, but 96% of the cases had aspiration of liquid consistency. Miller (1994) observed 33.3% of aspiration.

In our study, the occurrence of aspiration was associated with specific food consistency, but liquid consistency was more frequently aspirated (33.6%) than paste consistency (14.9%), according to Rogers (1994), Casas (1994), Bulcholz (1994), Casas (1995), Gisel (1995), Ranieri (1996) and Helfrich-Miller (1986), who found different results represented by higher aspiration of paste consistency. Frequent liquid aspiration may be justified because the viscosity of the bolus affects pharyngeal swallowing concerning duration of the contact of the base of the tongue and the pharyngeal wall, which is higher for paste bolus, according to Lazarus (1993). Kilman (1976) reported that severity may aid liquid pharyngeal transport, but viscous and solid materials are transported by muscle activity. Liquids tend to cause more stasis, and the flow is less coordinated and cohesive, requiring more muscle activity and more complex breathing/swallowing control.

Pathogenesis of aspiration and laryngeal penetration in children with cerebral palsy remains uncertain. Aspiration can be noticed before, during and after swallowing, and the cases can be related to each of these moments. Early leak of contrast into the pharynx, reduced movement of pharyngeal contraction, laryngeal structural alterations, abnormal coordination of oropharyngeal mobility and glottic closure and the presence of residues after swallowing can be associated with aspiration. However, there are a large number of children with these abnormalities that do not aspirate. The frequency of aspiration depends not only on pharyngeal phase-specific abnormalities, but also coordination of swallowing and breathing. In the present study, we observed pharyngeal tonsil hypertrophy in 94 children (43.1%); palatine and pharyngeal tonsil hypertrophy in 46 cases (21.1%); velopharyngeal insufficiency in 16 cases (7.3%); salivary stasis in 21 cases (9.7%); vocal folds paralysis in 9 cases (4.1%); presence of tracheostomy in 10 cases (4.6%), which contributed to the aggravation of swallowing and ventilation lack of coordination.

In the study, the presence of remains on the pyriform recesses and pharyngeal walls after swallowing was detected in 10 children (7.5%). Rogers (1993) found a frequency of remains of 60% in the assessment of five children with cerebral palsy. Wilson (1992) detected 66.6% of remains on the pyriform sinuses. Helfrich-Miller (1986) reported that in 100% of the cases (5 patients) there was remains on the vallecule and pyriform recesses. The stasis of residues in the pyriform recesses may be caused by a series of reasons, such as oral phase impairment and delay in propulsion of the bolus, delayed firing of swallowing reflex, reduced laryngeal elevation and dysfunction of the cricopharyngeal segment. Among them, we believe that the most commonly affected mechanisms in children with cerebral palsy are oral motor abnormalities and delayed firing of swallowing reflex.

Conclusion

After the functional assessment of swallowing using nasoendoscopic examination performed in 134 children with cerebral palsy and clinical presentation of oropharyngeal dysphagia, being treated at AACD, we concluded that:

1. Fiberoptic endoscopic assessment in children with cerebral palsy enables anatomical and functional assessment of the affected structures in the swallowing process, enabling the detection of essential information to the diagnosis and treatment of dysphagia;

2. Children presented high levels of impairment of the pharyngeal phase, and the most frequent abnormality was early leak of food into the pharynx, present in 72 patients (53.7%);

3. Tracheal aspiration in studied children was more prevalent with liquid consistency, detected in 45 patients (33.6%), whereas paste consistency was aspirated by 20 patients (14.9%). It shows that examinations can guide the family to use a safer consistency for regular feeding, preventing tracheal aspiration and its consequences;

4. The other abnormalities of swallowing pharyngeal phase were: laryngeal penetration of paste contrast (4.8%), laryngeal penetration of liquid contrast (5.2%), remains after swallowing (7.5%) and absence of laryngeal sensitivity (12.7%);

5. Functional assessment of swallowing through nasofibroscopy is a safe method to be used in children, with no risks or complications.

References

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1 Doctorate studies under course, Discipline of Otorhinolaryngology and Human Communication Disorders, Universidade Federal de São Paulo, Escola Paulista de Medicina; Assistant Physician, Hospital do Servidor Público Estadual - Francisco Morato de Oliveira - São Paulo; Otorhinolaryngologist, Clinic of Dysphagia, AACD - São Paulo
2 Resident Physician, Service of Otorhinolaryngology and Head and Neck Surgery, Hospital Servidor Público Estadual, Francisco Morato de Oliveira - São Paulo; Volunteer Otorhinolaryngologist, Clinic of Dysphagia, AACD - São Paulo

Address correspondence to: Dayse Manrique - Rua Canário, 112 aptº. 61 Moema - São Paulo /SP 04521 - 005 - e-mail: daysemanrique@uol.com.br

AACD (Associação de Assistência à Criança Defeituosa) - São Paulo