Affiliations:
1 Division of Pediatric Respiratory Medicine,
Department of Pediatrics, University Hospital Son Espases, Palma de
Mallorca, Spain.
2 Health Research Institute of the Balearic Islands
(IdISBa). Department of Pediatrics. Palma de Mallorca, Spain.
3 Sleep Unit, Department of Pediatrics, University
Hospital Son Espases, Palma de Mallorca, Spain.
4 Division of Neonatology, Department of Pediatrics,
University Hospital Son Espases, Palma de Mallorca, Spain.
5 Research Unit, University Hospital Son Espases,
Palma de Mallorca, Spain.
Corresponding author :
Fernando Rafael Aguirregomezcorta.
Secretaría de Pediatría (planta +1). Carretera de Valldemossa, 79, 07120
Palma, Illes Balears.
Phone number: +34618368311aguirrefer77@gmail.com.
Grants and financial support : None
Keywords : Children, swallowing disorders, dysphagia, chronic
aspiration, fiberoptic endoscopic evaluation of swallowing
Running head : Fiberoptic endoscopic evaluation of swallowing
ABSTRACT
Background and Objectives : Swallowing disorders lead to chronic
lung aspiration. Early detection and treatment of aspiration in children
with dysphagia is important to prevent lung damage. Diagnosis of
aspiration, which may be silent, requires an instrumental study such as
fiberoptic endoscopic evaluation of swallowing (FEES). Despite its
usefulness, it is rarely practiced by pediatric pulmonologists. This
study aimed to evaluate the feasibility and utility of FEES performed in
the pediatric respiratory unit of a tertiary hospital, analyze the
clinical characteristics, endoscopic findings and proposed treatments,
and identify the factors associated with penetration or aspiration.
Methods : Medical records of 373 children with suspected
aspiration who were referred to the pediatric respiratory unit for FEES
were reviewed retrospectively. Clinical characteristics, FEES findings,
and the proposed treatments were analyzed.
Results : Aspiration was seen in 47.9% of the patients. The
most common associated conditions were neurological disease and
prematurity. The most frequently observed endoscopic finding was altered
laryngeal sensitivity (36.5%). Intervention was recommended in 54.2 %
of the patients. Complications were not seen during any of the
procedures.
Conclusions : The FEES procedure performed by pediatric
pulmonologists is a reliable method for diagnosing aspiration in
children. It can be safely executed by trained pulmonologists, and
significant endoscopic signs other than aspiration can guide in the
diagnosis and management recommendations.
INTRODUCTION
Chronic pulmonary aspiration due to swallowing disorders is defined as
recurrent aspiration of food, fluids, or saliva during the oropharyngeal
phase of swallowing. The increase in its incidence in recent years can
be attributed to prolonged survival of patients with different
comorbidities.
This condition affects around 1% of the children in the general
population1. However, its incidence is much higher in
premature infants or those with anatomical malformations,
encephalopathies, neuromuscular disorders, and genetic
alterations2-3. It comprises a wide spectrum of signs
and symptoms, including chronic cough, recurrent pneumonia, wheezing
with poor response to treatment, atelectasis, stridor, lung abscess,
chronic lung damage with bronchiectasis, and respiratory
failure4. The abovementioned symptoms are frequently
treated at all levels of care, ranging from the primary care
pediatrician to the pediatric pulmonologist and intensive care units.
Diagnosing chronic aspiration in pediatric patients is challenging.
There are significant implications in the event of a delay in diagnosis.
Symptoms such as coughing or other signs of aspiration are not always
present during swallowing. Therefore, an instrumental evaluation, such
as videofluoroscopic swallow study (VFSS) or fiberoptic endoscopic
evaluation of swallowing (FEES) is recommended for the diagnosis of
chronic pulmonary aspiration5.
The FEES technique has been described useful and feasible in pediatric
patients for more than 20 years6. Nonetheless, it is
not routinely used across all centers and countries7.
This is probably due to limited availability of specialists trained in
this procedure. Pediatric pulmonologists have the necessary tools and
the anatomical and pathophysiological knowledge to perform this
procedure and interpret the findings. However, many children remain
undiagnosed and some of them do not receive proper treatment until the
detection of chronic lung damage. Moreover, there are few studies in
which the correlation between various endoscopic findings and the
possibility of aspiration in pediatric patients has been extensively
studied.
Therefore, in this study, we aimed to analyze the clinical
characteristics, endoscopic findings, and proposed treatments in
patients who underwent FEES in the pediatric pneumology unit of a
tertiary hospital. We also intended to identify the factors associated
with penetration/aspiration.
MATERIALS AND METHODS
We conducted a retrospective review of data of children with suspected
chronic pulmonary aspiration, who underwent FEES at the pediatric
pneumology department of the University Hospital Son Espases, Palma de
Mallorca, Spain. The hospital serves a reference population of 1,149,460
patients, with 172,058 in the pediatric age group. Our study was
approved by the Ethics Committee of Research of the Balearic Islands (IB
3876/19 PI).
We included patients aged 0–18 years, who underwent FEES between
January 2006 and December 2018. In patients who underwent multiple
studies, the data of the first evaluation was considered. We obtained
the data using fiberoptic bronchoscope (FB), FEES database, and the
hospital database that includes the clinical, laboratory, and radiology
data of the patients.
The patient characteristics included were: age, sex, comorbidities, and
reason for referral. The FEES procedure was performed according to the
technique described by Langmore et al8. A pediatric
pulmonologist conducted the procedure with the help of a pediatric nurse
in the Endoscopy suite or the Pediatric/Neonatology Intensive Care
Units, without displacing the critical patients. A 3-hour fasting period
was maintained before the procedure. The procedure was explained to the
parents and their informed consent was obtained. Our study adhered to
the guiding principles of the World Medical Association Declaration of
Helsinki. A flexible pediatric FB (frequently used in other situations),
such as the Olympus BF-XP190® (3.1 mm outer diameter) or the Olympus
BF-N20® (2.2 mm outer diameter) was used. A pulse oximeter (Masimo®,
Neuchatel, Switzerland) was placed on the patient’s foot to monitor the
heart rate and oxygen saturation. In addition, a drop of
lidocaine/prilocaine was applied to the anterior nasal passage using a
cotton swab, thereby avoiding anesthesia of the posterior area. The
introduction of FB facilitated assessment of the following features: the
structural and functional anatomy of the hypopharynx and larynx, pooling
of secretions, and the sensitivity of larynx through air pulses or a
brief contact of the endoscope with the arytenoids. This procedure was
followed by a direct evaluation of swallowing. We added a drop of dye to
the food for easy viewing. Different textures are used (liquid, nectar,
pudding, cookie) depending on the patient’s age and previous tolerance.
Swallowing was observed and any abnormalities and residues were
recorded. On detecting laryngeal penetration or aspiration, the
pulmonologist performed different compensatory strategies, such as
changes in positioning or feeding rhythm, modifications in the utensils
(including bottle/nipple systems), or modifications in the viscosity of
the liquids (thickening of the liquids), with the FB retained in its
position. This enabled a direct assessment of the response to treatment.
The tests were videotaped and subsequently evaluated with the use of
slow motion.
The following variables were collected in a standardized report:
anatomic abnormalities, altered laryngeal sensitivity, pharyngeal
pooling of secretions, laryngeal penetration (appearance of secretions
or food in the laryngeal vestibule above the vocal cords), aspiration
(passage of secretions or food below the vocal cords), residue of the
bolus in the hypopharynx after swallowing, proposed treatment, and its
effectiveness. The post-FEES recommendations were recorded and
classified into the following categories: a combined treatment
comprising a change of positioning or feeding rhythms; addition of
thickeners; use of omeprazole or other proton pump inhibitors (PPIs);and
non-oral feeding.
Data are expressed as absolute and relative frequencies for the
categorical variables and median and interquartile range for the
non-normally distributed continuous variables. We conducted the
Chi-square analysis or Fisher’s test to determine the association of
penetration/aspiration with the categorical variables. We used the
Student t test or Mann-Whitney test for the quantitative variables.
Considering their inclusion when the probability of alpha error was
<0.1 or when it created a confusing effect on others, we
conducted a multivariate analysis on an exploratory basis by building a
model of logistic regression. This helped us to assess the association
of the clinical and demographic variables associated with aspiration. We
determined the goodness of fit using the Hosmer-Lemshow test. The IBM
SPSS (v22, NY, USA) was used for the statistical calculations.
RESULTS
A total of 472 FEES procedures were performed on 373 children with
suspected aspiration. The initial FEES done for each patient was
considered for the analysis.. The median age was 11 months (IQR, 3–39
months) and 58.4% of the patients were boys. Neurological disorders
(34.3%) and prematurity (28.3%) were the most frequent underlying
pathologies. A significant number of patients (19%) had no apparent
predisposing factors for aspiration. Table 1 summarizes the demographic
data and the comorbidities.
The most frequent indications for the procedure were signs or symptoms
of aspiration, such as choking, gagging, or coughing while feeding
(46.6%), followed by refusal or an aversion to ingest (26%) (Table 2).
We observed abnormal swallowing resulting in penetration/aspiration in
47.9% of the cases. This rate was similar in both children born at term
and those born premature (46.6% and 51.4%). Of the 71 patients without
any predisposing factors, 22.5% presented with penetration and/or
aspiration.
Altered laryngeal sensitivity (36.5%) was the most frequently observed
endoscopic finding, besides penetration. Table 3 outlines the
predominantly observed abnormal findings. Therapeutic action was
recommended in 54.2% cases following FEES. Treatment with thickeners
(25.5%) was the most frequent recommendation. Oral feeding was
contraindicated in 12.3% of the cases, thus recommending the use of a
nasogastric or gastrostomy tube (Table 4). There were no significant
adverse events associated with the procedures.
The multivariate logistic regression model revealed an independent
association between aspiration and the predisposing factor, with
alterations in laryngeal sensitivity (odds ratio [OR], 5.68; 95%
confidence interval [CI], 2.74–11.77), pharyngeal pooling (OR 11.2,
95% CI, 3.14–40.15), and post-deglutition food residues (OR 7.89, 95%
CI 4.02–15.49). Neurological conditions, including cerebral palsy,
mental delay, and encephalopathy were most significantly associated with
aspiration (OR 1.99; 95% CI 1.01–3.92), compared to those with no
relevant previous pathology. Table 5 summarizes the remaining risk
factors associated with aspiration.
DISCUSSION
This study examined the patient characteristics, endoscopic findings,
and proposed treatments in children with suspected aspiration, evaluated
by FEES in a pediatric pneumology unit.
We observed penetration or aspiration in nearly half of the cases. Our
data were similar to those obtained in other pediatric
studies9. Nonetheless, their incidence varies
according to the pathology and age group, and was found to be greater in
patients with neurological disorders10.
Our study included pediatric patients of all age groups and it needs to
be highlighted that a large proportion of these were premature children.
(105 of 373 patients). This reinforces the value of FEES in this
specific population with high rates of pulmonary
aspiration11, and its application in breastfeeding
infants12.
FEES does not affect regular swallowing. Pharyngeal contraction causes
white-out and completely might block visualization of all oropharyngeal
structures for a brief period. As a result, food bolus movement is not
directly observed. A close inspection of the glottis and sub glottis may
reveal the aspirated material. If not directly observed, other
endoscopic signs provide information about a possible impairment of
normal swallowing.
Pharyngeal pooling of secretions, which is always an abnormal finding
correlated the most with aspiration, with an OR of 11.2. Saliva
aspiration is probably the least frequently reported form of chronic
aspiration. Saliva contains potentially pathogenic oral microorganisms
which can alter the lung microbiome, if the amount aspiration is
significantly higher13. Moreover, it can cause
pneumonia14. Salivary aspiration observed during FEES
has also been associated with other radiological alterations, such as
bronchial thickening and atelectasis15. Salivary
aspiration in children with neurological disorders is generally caused
by a severe incoordination of swallowing and reduced sensitivity of the
laryngopharynx, rather than due to excessive production of saliva.
Correspondingly, our study revealed a substantial association between
impaired laryngeal sensitivity in children and aspiration (OR=5.6). This
can be associated with the frequent alteration of sensitivity in
children with dysphagia16, which could be attributed
to gastro-esophageal reflux17.
The presence of post-swallow residue in the vallecula and/or piriform
sinuses is an endoscopic sign indicating an abnormal clearance of the
alimentary bolus. Therefore, we identified its correlation with
aspiration, consistent with other studies18. This
might be the result of an altered pharyngeal constriction, tongue
retraction, or laryngeal displacement19.
Despite the significance of a good clinical evaluation prior to
endoscopic examination, its low sensitivity for aspiration
detection20 makes it relatively unhelpful for the
pediatric pulmonologist. Furthermore, the great frequency of silent
aspiration in pediatrics21 calls for the need of a
complementary instrumental study. VFSS and the FEES22are the two most recommended complementary studies. Several studies have
compared the diagnostic benefits of the aforementioned techniques.
Notwithstanding their similar specificities, FEES is slightly more
sensitive for detecting penetration, aspiration, and residues, compared
to VFSS23-24.
Despite the complementary nature of these techniques, FEES has the
following advantages: real food and drinks are used, there is no
restriction on the duration of the test; it can be repeated several
times during follow-up, parents can observe the study, and the equipment
used for the procedure is portable, allowing FEES to be performed in
intensive care units as well.
However, the absence of radiation is its primary advantage, particularly
in children and premature patients. The radiation dose in VFSS is
relatively low, between 0.2 and 0.85 mSv25. A chest
X-ray usually involves a receiving radiation of 0.02 mSv. Nonetheless,
the need to repeat studies during follow-up increases this radiation to
the equivalent of more than 30 chest X-rays26.
Seventy-four patients (19.8%) required follow-up with repeated FEES in
our study.
The multidisciplinary approach to dysphagia implies enormous variability
in the diagnostic methods used in the USA, Australia, and
Ireland27-29. Despite the highlighted advantages of
FEES, VFSS is reportedly the most widely used diagnostic method.
Approximately 36-40% of clinical assessments are followed by VFSS in
Canada and the USA, with a slight difference in Australia and Japan.
Other instrumental assessments, such as FEES are not used as frequently
as VFSS30.This can be due to different reasons
associated with endoscopy, such as the non-availability of equipments,
lack of knowledge of the technique, lack of specialists, or different
legislations that regulate handling of the endoscope.
FEES is usually performed by otolaryngologists or speech pathologists in
the US, Japan, Canada, and some European countries19.
However, it is also performed by neurologists in other countries such as
Germany31.The ideal assessment of dysphagia should be
done by a multidisciplinary team. Pediatric pulmonologists are skilled
in flexible endoscopy and in the identification of structural and
functional abnormalities of the airway. This provides an optimal setting
for FEES examinations. Furthermore, they have the advantage of being one
of the most qualified specialists to relate the findings to the
underlying medical problem. To this end, it would be desirable to carry
out standardized and specific complementary training in this area open
to all clinicians, as also proposed by other authors31. Adequate training ensures excellent safety of the
technique32.
We also found aspiration during FEES in a subgroup of patients, without
any predisposing factor or underlying pathology. The abovementioned
findings have been previously reported33. Nonetheless,
the possibility of aspiration in this population is underestimated.
Our study has several limitations. First, the retrospective and single
center design made it susceptible to selection bias. Second, the patient
sample was heterogeneous. Therefore, it might create difficulty while
extrapolating our results to concrete patient populations. Nevertheless,
the variability of the pathologies and ages represents the kind of
patients commonly encountered in a pediatric hospital. Third, we
attempted to adjust for the important medical conditions that increase
the risk of aspiration. However, we may have not accounted for other
confounding factors. For example, despite similar neurologic comorbidity
labels in several patients, they might have extremely different
functional realities.
In conclusion, performing FEES in a pediatric pneumology unit is useful
and safe. Almost half of our patients who underwent FEES suffered from
penetration/aspiration. Direct or indirect identification of aspiration
is within the reach of pediatric pulmonologists with prior training.
This in turn will enable early diagnosis and avoid advanced lung damage.
In addition, it will provide information on the efficacy of compensatory
swallowing strategies and guide treatments.
Conflicts of interest : The authors declare no conflict of
interest.
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