Pediatric Pulmonology 47:321337 (2012)

State of the Art

Dysphagia and Aspiration in Children

James D. Tutor, MD1* and Memorie M. Gosa, CCC-SLP, BRSS2
Summary. Aspiration is a signicant cause of respiratory morbidity and sometimes mortality in
children. It occurs when airway protective reexes fail, especially, when dysphagia is also pres-
ent. Clinical symptoms and physical ndings of aspiration can be nonspecic. Advances in
technology can lead to early diagnosis of dysphagia and aspiration, and, new therapeutic
advances can signicantly improve outcome and prognosis. This report rst reviews the anato-
my and physiology involved in the normal process of swallowing. Next, the protective reexes
that help to prevent aspiration are discussed followed by the pathophysiologic events that
occur after an aspiration event. Various disease processes that can result in dysphagia and
aspiration in children are discussed. Finally, the various methods for diagnosis and treatment
of dysphagia in children are reviewed. Pediatr Pulmonol. 2012; 47:321337.
2011 Wiley Periodicals, Inc.

Key words: aspiration; dysphagia; pediatrics.

Funding source: none reported.

INTRODUCTION the current methods for diagnosis of dysphagia and its

Aspiration, the inhalation of foreign material into the
lower airway, has been a signicant cause of morbidity
and mortality throughout history. Aspiration can be an
acute event or a chronic recurrent syndrome. It may oc-
cur during oral feeding or may occur after feeding dur-
ing episodes of gastroesophageal reux (GER).
Aspiration may occur in children who have problems
with dysphagia, difcult or improper swallowing of
liquids, solids, or even saliva. When aspiration is chron-
ic and recurrent, the effects on lung development can
be devastating leading to pulmonary problems such
as recurrent wheezing, recurrent pneumonias, and the
development of severe impairment of lung function and
pulmonary scarring that can occasionally lead to death.
Though the exact incidence of dysphagia in children
and accompanying aspiration, is unknown, it is felt
to be signicant and it is frequently unrecognized
by primary care physicians or caregivers as a cause of
chronic respiratory symptoms.
In this article, dysphagia in children will be
reviewed. First, the normal swallowing mechanism and
the protective airway reexes to prevent aspiration will be
discussed. Next, the pathophysiologic events that occur
due to aspiration will be reviewed and some of the
disease processes in children that may be accompanied
by dysphagia are each briey discussed. Finally,
therapy, both current and evolving (including special
therapies for salivary aspiration), will be discussed.
ANATOMY AND PHYSIOLOGY OF SWALLOWING
To understand how aspiration can occur, knowledge of
the normal anatomy and physiology of the human swal-
lowing mechanism is required. Bosma made signicant
contributions to the current knowledge of the anatomy
of the head and neck in the infant and about its physio-
logic inuence on feeding and swallowing.13 The
1
Program in Pediatric Pulmonary Medicine, University of Tennessee
Health Science Center, LeBonheur Childrens Hospital, St. Jude Child-
rens Research Hospital, Memphis, Tennessee.
2
Speech Therapy Department, LeBonheur Childrens Hospital, Memphis,
Tennessee.
*Correspondence to: James D. Tutor, MD, Division of Pulmonology,
Department of Pediatrics, LeBonheur Childrens Hospital, 50 North
Dunlap, Memphis, TN 38103. E-mail: jtutor@uthsc.edu
Received 25 February 2011; Accepted 11 August 2011.
DOI 10.1002/ppul.21576
Published online 18 October 2011 in Wiley Online Library
(wileyonlinelibrary.com).

2011 Wiley Periodicals, Inc.

322 Tutor and Gosa
swallowing mechanism is part of the upper aerodiges-
tive tract which includes the oral, pharyngeal, and nasal
cavities and the larynx. All of these structures working
in a coordinated fashion are responsible for normal res-
piration, swallowing, and eventually speech.4 Infants
upper aerodigestive tracts are unique in their anatomic
relationships.46 The major anatomical differences are
presented in Table 1 and Figure 1a,b. These anatomic
differences in the infant are believed to provide the op-
timal arrangement for safe, effective nipple feeding.4
The anatomy of the newborn swallowing mechanism
gradually changes over the rst months of life as the
larynx descends in the pharynx and the upper aerodi-
gestive tract begins to resemble more closely that of the
adult by approximately 5 months of age. Sasaki et al.7
reported on the effects of laryngeal descent pointing out
that it allows for oral tidal breathing in the infant and
also coincides with the peak incidence of sudden infant
death syndrome (SIDS). As the larynx descends, it
allows for greater variety of vocalizations but the more
caudal laryngeal positioning sacrices the aspiration
protection believed to be afforded to the young infant
by the intranaral positioning of the epiglottis during
swallowing. Intranaral epiglottic positioning is only
possible with the most cephalic positioning of the lar-
ynx with the tip of the epiglottis at the level of cervical
vertebrae C2C3.8
For diagnostic purposes, swallowing is divided into
three distinct phases: oral (to include both oral prepara-
tory and oral transit phases), pharyngeal, and esophage-
al. What is functional for each of these swallowing
phases depends on the individual development of the
patient at the time of the assessment. Each of the three
phases plays a part in directing a bolus of salivary
secretions or ingested food into the esophagus, and not
into the air passages.9
AIRWAY PROTECTIVE REFLEXES
The airway is protected from aspiration by a series of
reexes with sensors in the pharynx, larynx, and esoph-
agus. These mechanoreceptors and chemoreceptors are
TABLE 1 Major Oral-Facial Anatomical Differences in Infants and Adolescents
Anatomic location Infant
Oral cavity Smaller, due to size and position of mandible
Filled with tongue and fat pads
Tongue Housed entirely in the oral cavity
Larynx Approximately 1/3 the size of the adult larynx,
minimal gender differences
Vocal fold length is 2.53.0 mm
Epiglottis Tip is located at C2
Tip makes contact with soft palate
Eustachian tubes Located at the floor of the nasal cavity
Pediatric Pulmonology
concentrated over the surface of the pharynx, epiglottis,
arytenoid cartilages, and vocal cords.10,11 The chemore-
ceptors are activated by water, as well as by a variety
of salts, sugars, and acids.12,13 Failure of these protec-
tive reexes allows aspiration to occur from swallowed
boluses or material reuxed up the esophagus from the
stomach.
The nature of the protective reex response invoked
varies as a function of the age of the individual and
the region of the pharynx or larynx that is stimulated.
Mechanical stimulation of pharyngeal afferent receptors
stimulates swallowing at any age. In susceptible human
infants, stimulation of the laryngeal chemoreex, when
acid, water, or milk contacts the larynx, can lead to pro-
longed apnea, rather than coughing and swallowing.
This developmental inuence is most likely due to cen-
tral respiratory inhibition.14 Viral respiratory infections
can cause the adult response pattern, that is, coughing
and swallowing, to revert to the immature pattern
in which apnea predominates.15 This tendency may
explain why prone infants with respiratory viral infec-
tions, such as respiratory syncytial virus (RSV), have
an increased incidence of apnea and SIDS particularly
when lying face downward.1618 When studied in detail,
in a premature and a term infant, each experiencing
apnea while infected with RSV, the spontaneous apneic
events resemble laryngeal chemoreex-associated apnea.
The apnea event in the RSV-infected infants often
lasted longer than 30 sec. The apnea was rst central
and then obstructed (i.e., mixed) and was usually termi-
nated after a series of swallows, or occasionally a
cough. Upper airway secretions, which are increased
during acute RSV infection, might elicit prolonged
laryngeal chemoreex-associated apnea unless cleared
efciently by swallowing.17,18
Thach19 discussed the maturation of cough and other
reexes in the neonatal airway. Maturation of the laryn-
geal cough response leads to an increase in coughing
and a decrease in both swallowing and apnea. These
changes have been attributed to central processing of
afferent (sensory) stimuli as opposed to a reduction in
the sensitivity of the larynx or any major change in the
Adolescent
Larger, due to downward forward growth of mandible
Presence of teeth and absence of sucking pads creates more space
Base of tongue is located in the oropharynx
Vocal fold length is 1721 mm
Size of the adult larynx is 36 mm for females and 44 mm for males
Tip is located at C57
Tip no longer makes contact with soft palate
Located posteriorly to the inferior nasal conchea

Fig. 1. a: The mouth and pharynx of the adult. b: The mouth
and pharynx of the newborn. The anatomical parts begin to
change over the 1st months of life so that by age 5 months,
the anatomy is much closer to that of the adult. Figure used
by permission of Betsy True, New Visions, and Suzanne E.
Morris, PhD.
distribution or quantity of receptor sites within the lar-
ynx. Laryngeal chemoreceptors in the newborn are the
primary defense against aspiration of liquids. As the in-
fant matures, the laryngeal cough response (reex)
becomes more prominent. In adults, the chemoreexive
responses of the larynx continue to provide the primary
source of airway protection.19
Dysphagia in Children 323
During most episodes of GER, the gastric contents
enter the lower esophagus, but the upper esophageal
sphincter remains closed. The reuxed gastric contents
are pushed back into the stomach by peristaltic contrac-
tions in the body of the esophagus.20 During these epi-
sodes of GER, some patients may cough, even though
the gastric contents do not enter the pharynx. This
coughing may be due to a reexive increase in salivary
secretions that occurs after esophageal acid exposure.21
Patients with abnormal airway anatomy or inadequate
stimulation of swallowing may have difculty handling
the increased volume of salivary secretions and there-
fore aspirate saliva, causing a cough.20 In addition, acid
exposure of the esophagus can result in apnea22 or
bronchoconstriction.23 When the proximal esophagus is
distended vigorously, the upper esophageal sphincter
relaxes and allows reuxed stomach contents to enter
the hypopharynx.20 Closure of the airway occurs as
a result of stimulation of the esophagoglottal closure
reex. This reex causes anterior movement of the
larynx, closure of the vocal cords, and apnea in a man-
ner similar to that seen with swallowing.20,24,25 If the
reuxed gastric contents enter the pharynx, they are
expelled from the mouth or swallowed before respira-
tion is reinitiated. The afferent information that stimu-
lates this reex is carried in the recurrent laryngeal
nerves.20,26,27
PATHOPHYSIOLOGIC EVENTS ASSOCIATED
WITH ASPIRATION
Aspiration has the potential to cause permanent dam-
age to the developing lungs of infants and children.
Teabeut28 suggested that as the pH of aspirated material
drops below 2.5, lung injury increases, with maximal
lung injury occurring at a pH of 1.5. The volume of the
aspirated material also plays a major role in lung injury.
In dogs, 1 ml/kg of acid aspiration produces only mild
effects, whereas 2 ml/kg or more of acid aspirate causes
serious effects, usually death.29 Histologic ndings of
aspiration include degeneration of bronchiolar epitheli-
um, pulmonary edema and hemorrhage, focal atelecta-
sis, exudation of brin, and acute inammatory cell
inltrate. Later ndings include regeneration of bron-
chiolar epithelium, proliferation of broblasts, and
brosis.30 Gastric contents instilled into the trachea of
dogs appear on the lung surface within 1218 sec.
Extensive atelectasis develops within 3 min. Changes
of acute pneumonia occur within hours, and granuloma-
tous changes develop within 48 hr.31,32
Aspiration is most commonly the result of dysphagia
(swallowing dysfunction), gastroesopheageal reux disease,
or insufcient management of nasal/oral secretions.33
There are several conditions that predispose children to
aspiration lung injury (Table 2).
Pediatric Pulmonology
324 Tutor and Gosa
TABLE 2 Conditions Predisposing to Aspiration in over time with growth and further neurological develop-
Children ment. Sheikh et al.41 reported on a group of neurologi-
Anatomic cally intact infants born at term without GER who
Choanal stenosis had chronic aspiration due to dysphagia that resolved
Cleft lip/palate
within 39 months.
Laryngotracheal cleft
Esophageal atresia Dysphagia with aspiration can also occur in young
Tracheoesophageal fistula infants due to fatigue of the swallowing mechanism
Craniofacial abnormalities during feedings. This frequently occurs when the
Vascular ring infants are pushed to take prolonged or large feedings,
Tumors
particularly toward the end of the feedings.34 Infants
Cystic hygroma
Syndromes placed in their beds with bottles propped in their
Pierre-Robin mouths are at risk for dysphagia and aspiration, espe-
Beckwith-Wiedemann cially when they try to suck and swallow when only
Down (sometimes) partially awake.42
Neuromuscular
Young infants who develop viral respiratory illnesses,
Perinatal asphyxia
Cranial nerve or recurrent laryngeal nerve injury such as RSV bronchiolitis, may develop silent aspira-
Congenital hydrocephalus tion.31 This can lead to unexpected acute respiratory
Neonatal intraventricular hemorrhage deterioration if these infants continue to eat by mouth.
Familial dyautonomia Providing thickened feedings to these infants during the
Moebius syndrome
course of their bronchiolitis has been suggested.43
Myotonic dystrophy
Wernig-Hoffman disease Anatomic problems involving the nasopharynx,
Cornelia de Lange syndrome oropharynx, and trachea can result in dysfunctional
Muscular dystrophy swallowing with resultant aspiration. In some infants
Myasthenia gravis with choanal stenosis, respiratory distress may occur
Guillian-Barre syndrome
only with oral feedings. Due to increased nasal resis-
Cerebral palsy
Vocal cord paralysis tance to airow and the infants necessity for nasal
Arnold-Chiari malformation (sometimes) breathing, the infant cannot adequately coordinate suck-
Gastrointestinal ing and swallowing with breathing.34 Treatment con-
Gastroesophageal reflux sists of complete repair of these anatomic abnormalities
Esophageal motility dysfunction
with operative intervention if the infant is free of other
Other
Developmental/immaturity of swallowing serious medical conditions or with placement of a
Respiratory syncytial virus bronchiolitis tracheostomy if surgical repair is not appropriate or
Endotracheal tubes/tracheostomy tubes feasible.4446
Foreign body aspiration Infants with cleft palates and lips are at risk for aspi-
Collagen vascular disease
ration due to nasal reux of feeding causing them to
Obstructive sleep apnea
Bottle-propping gasp and have aspiration.34 Also, aspiration may occur
if food in the nasal cavity falls into a still open airway
The major differences of the VFSS and FEES/FEESST examinations after the infant has swallowed. Treatment includes
are outlined in Table 3. proper positioning of the infant during feeding, allow-
ing only short bursts of sucking, suctioning the airway
during feeding, and providing supplemental oxygen to
CAUSES OF DYSPHAGIA
the infant during feeding, if needed. Another treatment
The acquisition of the ability to swallow in a normal of the feeding problems of an infant with a cleft
fashion is a developmental phenomenon. Premature palate requires identication of a therapeutic bottle
infants are at signicant risk for dysphagia but by and nipple system that will ensure adequate oral intake
34 weeks gestation the swallowing mechanism has gen- despite the childs poor capacity for sucking.
erally developed adequately enough so that they are Laryngotracheal clefts, esophageal atresia, and tra-
able to transition from gavage feedings to oral feedings cheoesophageal stulas (TEFs) can result in aspiration.
given by breast or bottle.34,35 If there is incomplete de- Infants with laryngotracheal clefts, esophageal atresia,
velopment or coordination of the suckswallowbreathe and TEFs are at risk for respiratory difculties, such
mechanism, aspiration due to dysphagia can occur.36,37 as coughing, choking, cyanosis, or respiratory distress
Often this problem occurs in association with a linger- in association with feeding, and feeding may precipitate
ing neonatal respiratory illness with or without the pres- aspiration with the subsequent risk of recurrent
ence of tachypnea.3840 Occasionally, infants born at pneumonia.47 Preoperative therapy involves maintaining
term may have dysphagia, but this seems to improve a patent airway and preventing aspiration of secretions
Pediatric Pulmonology

and gastric contents. Denitive treatment is surgical
repair, with closure of the laryngotracheal cleft, division
and ligation of the TEF, and end-to-end anastomosis of
the esophagus, if feasible.47
Infants and children with craniofacial abnormalities
that include micrognathia or macroglossia can have
problems with recurrent aspiration. The presence of
micrognathia results in relative macroglossia that com-
promises the oral airway and often interrupts, impairs,
or prevents successful oral feeding.34 The infants should
be maintained in the prone position so that the tongue
and mandible fall forward to relieve airway obstruction
at the tongue-base level.48 When positioning alone fails,
tongue-base airway obstruction may be relieved by
placement of a nasopharyngeal airway without anesthe-
sia.49 However, in that same study, of the 35 infants
who had placement of nasopharyngeal airways, 40%
ultimately needed tube feedings suggesting that airway
interventions may negatively affect feeding perfor-
mance.49 In some infants, tongue-lip adhesion surgery
pulls the tongue anteriorly in the oral cavity, opening
the posterior pharynx, thus enabling them to grasp the
nipple and to successfully suck and swallow and to ex-
perience unobstructed breathing.34,50Adverse outcomes
of that surgery include dehiscence and need for sub-
sequent procedures.51 Some have argued that tongue-
lip adhesion is detrimental for feeding because it
alters tongue mobility and swallowing while others
have found improved feeding and weight gain after
glossopexy.52,53 Mandibular distraction procedures in
the neonate can improve mandibular size, enhance
respiration, and facilitate oral feedings.48,54
Infants with Down syndrome have protruding
tongues and occasionally cleft palates or tracheosopha-
geal stulas that can put them at risk for feeding dif-
culties and aspiration. Also, Wells et al. reported on
patients with Down syndrome who had midtracheal
stenosis. These patients had respiratory difculty and
stridor.55 Infants with short tracheas would seem to be
at high risk for aspiration.
Infants with left-sided congenital diaphragmatic her-
nia (CDH) have a high incidence of GER, 22%81%,56
which could place these infants at possible risk of aspi-
ration. GER is most commonly seen in infants who
have had patch closure of their CDHs or if the stomach
was located in the thorax.57 If these predictors are pres-
ent, performance of a fundoplication at the time of re-
pair of the CDH may help in controlling GER.58,59
However, long-term follow-up for GER in CDH survi-
vors is mandatory.57
Vascular rings and pulmonary slings are well-dened
congenital anomalies of the aortic arch, brachiocephalic
arteries, or pulmonary arteries that cause symptoms
due to compression of the airway, esophagus, or both.60
Respiratory symptoms, such as stridor, barking cough,
Dysphagia in Children 325
and wheezing, predominate, but dysphagia may be pres-
ent as well. Surgical intervention is generally required.
Infants and children with neurologic or neuromuscu-
lar dysfunction may develop aspiration. They may be
unable to feed by nipple or at the breast due to an
inability to coordinate breathing and swallowing, or
because they lack adequate bulbar muscle function to
successfully feed.34 They also may have a weak gag
mechanism or ineffective cough that predispose them to
acute and chronic aspiration.30 Infants who have a dif-
cult vaginal delivery of their heads with the possibility
of a cranial nerve or laryngeal recurrent nerve injury,
or infants who have perinatal asphyxia, congenital
hydrocephalus, or neonatal intraventricular hemorrhage
should also be screened for the presence of feeding dif-
culties by observation of their feeding by a feeding
team that includes a feeding therapist with subsequent
testing for dysphagia, if needed.34
Aspiration can occur in infants and children with en-
dotracheal tube placement or with tracheostomies. En-
dotracheal tubes can cause remodeling of the palate due
to pressure of the tube on the hard and soft palate. After
extubation, the infant may be unable to establish a seal
around the nipple during feeding due to palato-pharyn-
geal incompetence, leading to aspiration secondary to
nasal reux of feedings or defective integration of the
sucking and swallowing mechanism.61 The presence of
a tracheostomy tube interferes with the swallowing
mechanism by preventing the subglottic rise in tracheal
pressure and by limiting elevation of the larynx during
swallowing.6264 The use of a one-way speaking valve
has been shown to improve swallowing function in
adults and children with a tracheotomy by improving
oral and pharyngeal sensation and increasing subglottic
pressure during swallowing. The use of these speaking
valves have been shown to decrease the occurrence of
aspiration in adults.65 The use of a tracheostomy tube
with an inatable cuff has previously been used by
some to hopefully decrease the risk of aspiration of
oral liquids and feedings in some children who have
dysphagia. Currently, it is recommended that the cuff
not be inated during eating so as not to tether the lar-
ynx and prevent its rise.66 Care must be taken to not
overinate the cuff of these tubes or leave the cuffs
continuously inated since that may lead to ischemia of
the tracheal mucosa sometimes with disastrous results
such as formation of a TEF or a trachea-innominate ar-
tery stula.6769
Acute episodes of aspiration can occur when infants
or children swallow volatile or oily liquids such as
mineral oil, medium-chain triglycerides, furniture
polish,70,71 or other hydrocarbon-containing liquids.
These liquids cause extensive airway mucosal and lung
parenchymal inammation and injury, resulting in
pneumonia with the possibility of acute respiratory
Pediatric Pulmonology
326 Tutor and Gosa
distress syndrome,72 and pulmonary parenchymal bro-
sis.73 Infants and children, particularly those younger
than 4 years old, are at the highest risk to acutely aspi-
rate foreign bodies. Also, older children occasionally
aspirate foreign bodies. However, the relative risk and
the types of foreign bodies that are aspirated change.
This can result in asphyxiation and death or post-
obstructive pneumonia and eventually bronchiectasis.34
SYMPTOMS OF ASPIRATION
Aspiration may occur due to dysphagia, in children
with some neurological conditions or with weak muscu-
lature, or in those with disorders of gastroesophageal
motility and sphincter tone. They may present to their
physicians with complaints such as wheezing that is
poorly responsive to appropriate therapies, chronic
cough, recurrent pneumonia, atelectasis, bronchiectasis,
pulmonary abscess, pulmonary brosis, bronchiolitis
obliterans, apnea/bradycardia/acute life-threatening events,
failure to thrive, stridor, or laryngitis/hoarseness.74
Animal studies have suggested that microaspiration can
cause symptoms directly from airway inammation as
well as predisposing to or accentuating airway hyperre-
activity. Reex bronchoconstriction from esophageal
acidication has been observed in both animals and
humans.74,75 Esophageal acidication can also increase
nonspecic airway hyperreactivity without necessarily
causing a change in baseline pulmonary mechanics.76
Infants and children with an absent or ineffective
cough reex may have silent aspiration and have nd-
ings of only increased respiratory mucus, congestion
and chronic wheeze or rhonchi, recurrent bronchitis, or
recurrent pneumonia.34,77
PHYSICAL EVALUATION FOR ASPIRATION
It is important that the clinician observe the infant
or child eating and auscultate the chest and back both
before and after feeding for crackles, wheezes, wet
upper airway noises, and wet voice quality. Attention
should be given to nasopharyngeal reux, difculty
when sucking or swallowing, and associated coughing
and choking. Drooling or excessive accumulation of
secretions in the mouth suggests dysphagia.78
RADIOGRAPHIC EVALUATION OF ASPIRATION
The initial test for a patient with chronic or recurrent
respiratory symptoms often is the chest radiograph. In a
group of 22 children with recurrent aspiration, the chest
radiograph was normal in 14% and revealed only bron-
chial wall thickening or hyperination in 18%. The
radiographs in the rest of the children revealed diffuse
(27%) or localized (41%) inltrates. Inltrates in infants
with recurrent aspiration can be in dependent areas
Pediatric Pulmonology
such as the upper lobes and the posterior areas of the
lower lobes.30 Inltrates are frequently not associated
with fever typical of infectious causes. Chest radio-
graphs are largely insensitive to early changes of lung
injury.79
Computed tomography scans, particularly high-reso-
lution images, are more sensitive in the detection of
early airway and parenchymal disease in children who
aspirate, particularly in those with lipoid pneumonia.80
Findings of bronchial wall thickening, air-trapping,
bronchiectasis, ground-glass opacities, and centrilobular
opacities (tree in bud) are common in children who
chronically aspirate.33
DIAGNOSIS OF CHRONIC ASPIRATION DUE
TO DYSPHAGIA
The pediatric assessment for dysphagia begins with
a thorough review of the patients history, including
medical, developmental, and feeding history.8083
Clinical feeding assessment usually includes obser-
vation of the parent and child during feeding, oral
peripheral examination, communicative behavior, and
observations of the child before and after feeding.8183
It may also include a screening test for aspiration such
as the 3-ounce water swallow challenge (3-oz WSC).84
Suiter et al.85 reported on the sensitivity and specicity
of the 3-oz WSC for children ranging in age from 2 to
18 years of age. They utilized the results of beroptic
endoscopic evaluation of swallowing (FEES) as the out-
come variable and standard by which the results of the
3-oz WSC were compared. The sensitivity for predict-
ing aspiration using the 3-oz WSC was 100% with a
specicity of 51%. The sensitivity and specicity of the
3-oz WSC for predicting which children could safely
intake thin liquids was 100% and 44% respectively.
Based on these results, the authors suggested that suc-
cessful accomplishment of the 3-oz WSC allows for the
safe oral intake of thin liquids as well as pureed and
soft oral solids without the need for further swallowing
assessment. They did suggest, however, that the 3-oz
WSC was not the best screening tool for identifying
children who are at risk for aspirating thin liquids due
to the high false positive rate and low specicity of the
test.85
Instrumental assessment is necessary for denitive
diagnosis of swallowing dysfunction and aspiration.86
Instrumental assessment for dysphagia might include
the following: videouoroscopic swallow study (VFSS),
also commonly known as the modied barium swallow
study (MBS), beroptic endoscopic evaluation of
swallowing with or without sensory testing (FEES or
FEESST), sonography, manometry, scintigraphy, and
cervical auscultation.8183,87 VFSS and FEES/FEESST
are the most common instrumental assessments for
 Dysphagia in Children 327
TABLE 3 VFSS Versus FEES/FEESST

Component VFSS FEES/FEESST

Visualizes Radiographic image of oral cavity, pharynx, larynx, trachea,
and upper esophagus during all four stages of the swallow
in real time
Test materials Small amounts of barium liquids, semi-solid barium
consistency, and solid consistency with barium coating
Duration Limited to 24 min due to use of fluoroscopy
Soft tissue components of pharynx and larynx before and
after swallow, including any soft tissue anomaly; unable
to visualize pharynx during the swallow due to white-out
with pharyngeal constriction during swallow
Real food items colored to provide contrast
Duration of entire meal (if necessary)

objective assessment of oropharyngeal swallowing in the pediatric population. It continues to be the

function in the pediatric population (Table 3). Neither
procedure has been established as a gold standard
for the detection of aspiration. Rao et al.88 compared
VFSS and FEES to determine their sensitivities and
specicities. When each was individually used as a
gold standard for the detection of aspiration, FEES
was found to have a higher sensitivity, but VFSS was
found to have a higher specicity in their study
(Table 4). Several investigators have reported on the
reliability of FEES as compared to other diagnostic
tests for aspiration, primarily VFSS in pediatric popula-
tions and have found it to be a reliable and safe exam
for diagnosing dysphagia. It has good agreement with
VFSS in that population, especially when trying to
detect aspiration.8993 However, currently data is only
available in adults, not in children regarding the sensi-
tivity and specicity of FEES to detect aspiration
(Table 4).
VFSS
The VFSS is the only instrumental assessment that
provides visualization of the anatomy of the oral cavity,
pharynx, larynx, and upper esophagus, as well as the
function and integration of all four areas during the
dynamic process of swallowing. It provides the most
thorough assessment of swallowing function and of
compensatory measures to improve swallowing function
assumed gold standard in adults for objectively
assessing oropharyngeal swallowing function. VFSS is
generally considered to be a reliable and safe method
for diagnosing dysphagia in the pediatric population.
The test, however, potentially employs a signicant
amount of radiation exposure to the brain. The benets
from use of the test should be weighed against its risks,
particularly if its use involves small infants or in chil-
dren with signicant brain injuries. Currently, no data
is available regarding its sensitivity and specicity
for detecting aspiration in children and, only one
study has reported on its sensitivity and specicity in
adults.33,8183,9497
VFSS is accomplished by age/developmentally
appropriate positioning of infants and children within
a uoroscopy suite in a specialized seating device
that provides adequate trunk, neck, and head control.
Presentation of test materials and viscosity of test mate-
rials are also presented in an age/developmentally
appropriate format.82
For infants younger than 6 months, liquid from a bot-
tle is presented. For infants older than 6 months and
children, liquid is given from a preferred method (in
graded quantities if cup/straw drinking), and thicker
consistencies and chewable foods are offered when
developmentally appropriate.82
The ultimate goal of the VFSS is to determine the
physiologic cause of the dysphagia symptom (aspiration

TABLE 4 Sensitivity and Specicity of Tests to Detect Aspiration

Comparative
Measure measure Sensitivity Specificity Refs.

Fiberoptic endoscopic evaluation
of swallowing (FEES)
Videofluoroscopic Swallow
Study (VFSS)
Lipid-laden macrophage
index (LLMI)
Blue dye test (BDT)
Modified Evans blue
dye test (MEBDT)
VFSS 7096% for detecting 87.5100% for detecting 88,89,9093
aspiration in adults aspiration in adults
FEES 100% for detecting 63% for detecting aspiration 88,9496
aspiration in adults in adults
Battery of other clinical 6998.6% for detecting 7879% for detecting aspiration 105107
and imaging exams aspiration in infants in infants and children
and children
VFSS 3879% for detecting 28100% for detecting 124,126132
aspiration in adults aspiration in adults
FEES 8295% for detecting 38100% for detecting 124,126,127,128132
aspiration in adults aspiration in adults

Pediatric Pulmonology
328 Tutor and Gosa

or laryngeal penetration, nasopharyngeal backow, reported that children with suspected aspiration had an
swallow trigger, and pharyngeal residual) and then LLM index >86, with the highest LLM index in the
identify the most appropriate treatment strategies to nonaspirator group being 72. Furuya et al.106
allow the safest and most appropriate intake of calories reported that a LLM index >165 had a 98.6% sensitivi-
for infants and children. When choosing management ty, 78% specicity, and 87.8% overall accuracy as a
strategies, the clinician must be mindful of the develop- diagnostic test for aspiration in a group of 112 children.
mental level of the patient as well as the patients A LLM index >90 for aspirators versus nonaspira-
cognitive status.82,97 tors, was retrospectively reviewed in 1999. The sensi-
tivity and specicity of the test were 0.69 and 0.79,
FEES/FEESST respectively.107 Elevated LLM indexes have been found
in children, not suspected of aspirating who have vari-
FEES enables direct visualization of soft tissue struc-
ous diseases including cystic brosis, those receiving
tures before and after the swallow.33,98 For infants and
intravenous lipid preparations, those with pulmonary fat
children, the speech-language pathologist or physician
embolism in sickle cell disease, and those with endogenous
passes a small exible endoscope through the patients
lipoid pneumonia from bronchial obstruction.108112
nose and positions it for optimal visualization of the
The LLM index is reportedly poorly reproducible due
hypopharynx and larynx. Test materials are colored to
to inter- and intra-observer variability in calculating the
provide improved visualization of the foods and liquids
index.113 Finally, the LLM index may also vary depend-
as they are swallowed.99
ing on the amount of time since the last aspiration
During feeding, FEES can identify oropharyngeal
event.114 Despite all these limitations, a LLM index
dysfunction that occurs before the swallow such as
may provide supporting evidence of aspiration in select
spillover and laryngeal penetration or aspiration. During
patients.115
the swallow, pharyngeal constriction causes white-out
Some children may have aspiration of saliva with
and briey totally blocks all visualization of oropharyn-
continued respiratory symptoms even if other causes of
geal structures. After the swallow, residual material can
aspiration from oral feeding and GER have been effec-
be seen, and the presence of laryngeal penetration or
tively treated. The radionuclide salivagram is used to
aspiration from the residue can be noted. Additionally,
try to detect salivary aspiration. A small quantity of ra-
aspiration during the swallow may be identied with
diotracer is placed in the buccal pouch, and serial
visualization of food or liquid in the trachea after the
images are taken until the tracer clears the mouth.
swallow.99 Treatment strategies can then be tested and a
Activity in the trachea or bronchi indicates aspiration.
treatment plan made based on information collected
Though it has been reported that the salivagram is
from the history, clinical feeding assessment, and
a sensitive test for salivary aspiration, there was only
FEES.
26%28% prevalence of positive salivagrams in chil-
FEESST gives the examiner information about swal-
dren suspected of aspiration seen in three retrospective
lowing dysfunction and about the laryngeal adductor
studies.116118 Salivagrams also have poor correlation
reex (LAR). The LAR, which is vital for airway
with other tests of aspiration such as barium video-
protection, is stimulated by providing controlled air
uoroscopy and milk scans.119 In a study evaluating the
pulses to the aryepiglottic folds through the port of
ability of salivagrams to predict the need for laryngotra-
a exible laryngoscope. By stimulating them with
cheal separation (LTS), there was no signicant correla-
increasing pressure in the form of the air pulse, the
tion noted between the salivagram result and days
examiner gains information about laryngopharyngeal
hospitalized due to respiratory symptoms.120 However,
mechanosensitivity. Normal LAR is elicited with
Finder et al.121 reported the use of serial salivagrams to
<4.0 mmHg of air pulse pressure; anything greater
titrate continuous positive airway pressure given via tra-
than that is considered abnormal. Abnormal laryngo-
cheostomy to decrease salivary aspiration. Thus, while
pharyngeal mechanosensitivity can result from a variety
the salivagram is useful for the detection of aspiration
of conditions, including GER disease.100104
in some patients, further studies need to be conducted
to evaluate its sensitivity and specicity. This has not
OTHER DIAGNOSTIC TESTS OF ASPIRATION
been done to date due to the lack of a gold standard
The calculation of a quantitative index of lipid-laden exam for detection of salivary aspiration to which the
macrophages (LLM) in bronchoalveloar lavage samples salivagram can be compared.
has been evaluated repeatedly as a test for chronic aspi- Colored dye placed on the tongue (blue dye test) or
ration, but results have been conicting (Table 4). mixed in the foods (modied Evans Blue dye test) of
Colombo and Hallberg105 reported on the use of an children with endotracheal tubes or tracheostomies was
LLM index in a group of children suspected to have previously frequently used to determine whether chron-
aspiration during feeding. Using a 0400 scale, they ic aspiration into the pulmonary airway is occurring
Pediatric Pulmonology

(Table 4). Finding of the dye in tracheal secretions suc-
tioned from the airway tube is presumptive evidence of
aspiration. Amanntea et al.122 reported on a group of 50
endotracheally intubated children who had Evans blue
dye placed in their oral cavities. Two tracheal aspirates
were obtained at 5-and 30-min intervals. The preva-
lence of aspiration was reported to be 28%.
Several researchers, who studied only adults, have
compared the accuracy of dye studies with other diag-
nostic studies of aspiration such as the VFSS and the
FEES. Four of the studies reported the false negative
rates of the dye studies to be 5061% but with specic-
ities near 100%. In those studies, food of various con-
sistencies for VFSS and FEES were dyed blue, and the
tracheostomy tube was then suctioned.123126 Belafsky
et al.127 reported on the use of a modied blue dye
screening protocol and found the modied Evans blue
dye test to have slightly higher sensitivity and specici-
ty for detecting aspiration than the unmodied blue dye
test (Table 4). Dye studies using large volumes and
more frequent administrations were previously reported
to serve as a screening test for children with possible
aspiration.79 Using either VFSS or FEES to document
aspiration, several reports have examined swallowing
function in pediatric patients with tracheostomies and
have reported on the incidence, prevalence, and symp-
toms of dysphagia found in this population. None of
these studies reported on the use of the blue dye test or
the modied Evans blue dye test in these children. Pres-
ently, data for determining the sensitivity and specicity
of the blue dye test or the modied Evans blue dye test
to detect aspiration in children is unavailable.128132
The use of these blue dyes in enteral nutrition formula-
tions has signicantly decreased or been discontinued
in many institutions due to reports of systemic absorp-
tion of the dye with the subsequent development of
adverse outcomes.133
PULMONARY FUNCTION TESTS IN INFANTS
WITH DYSPHAGIA
Sequelae of pulmonary aspiration associated with
dysphagia in children can include infections such as
pneumonias and pulmonary abscesses. Other children
can also develop chronic conditions such as bronchiec-
tasis, pulmonary brosis, or bronchiolitis obliterans.
When these conditions occur, they require treatment
and monitoring. One of the monitoring tools now avail-
able in infants with dysphagia is pulmonary function
tests (PFTs).
Recently, Tutor et al.134 performed (PFTs) in a group
of 18 neurologically normal infants, born at term, each
with a history of recurrent coughing and wheezing and
who had dysphagia newly diagnosed using VFSS. Thir-
teen of the infants also had concomitant documented
Dysphagia in Children 329
GER, and ve of the infants were also exposed chroni-
cally to tobacco smoke. The PFTs were performed
shortly after the diagnosis of dysphagia using the
raised lung volume rapid thoracoabdominal compres-
sion technique135,136 and consisted of pre- and post-
bronchodilator spirometry and measurement of lung
volumes via plethysmography. Twelve infants had
abnormal PFTs, with 11 demonstrating evidence of air-
ways obstruction (AO), 4 of whom also demonstrated a
component of bronchodilator responsiveness (BR) after
receiving albuterol. Ten of the original 18 infants under-
went a repeat PFT 6 months after initiation of therapies
for dysphagia and GER. Of the 12 infants who
had abnormalities on their initial PFTs, 3 infants contin-
ued to demonstrate AO without BR, and 2 infants con-
tinued to demonstrate AO with BR, respectively. One
infant who initially demonstrated AO without BR on
the rst PFT demonstrated normal spirometry but a
mild decrease in total lung capacity on plethysmogra-
phy 6 months later. Two of the infants with AO on their
initial PFTs had completely normal PFTs 6 months lat-
er. Eight of the 10 infants who performed PFTs initially
and 6 months later, had documented evidence of GER.
The initial PFTs of seven of those eight infants were
abnormal but 6 months later four of the seven infants
had normal PFTs. All ve of the infants who were
chronically exposed to tobacco smoke had abnormal
initial PFTS but 6 months later, three of those infants
had normal PFTs. The authors concluded that PFT
abnormalities, predominantly AO, occur commonly
in infants with respiratory symptoms who have been
recently diagnosed with dysphagia and many of the
infants continued to show abnormalities at follow-up.134
Performance of PFTs in infants diagnosed with dys-
phagia is suggested to determine if abnormalities are
present. They may need to be repeated, particularly if
the infants remain symptomatic despite appropriate
treatment of their dysphagia.
TREATMENT OF DYSPHAGIA
Initial decisions for the treatment of dysphagia must
take into account the prognosis for safe and adequate
oral intake. The safest, most effective method of
caloric intake may either be orally with compensatory
strategies or temporary/permanent feeding tube
placement.81,83
Compensatory strategies for infants and children
may include changes in positioning, changes/modica-
tions to utensils (including bottle/nipple systems),
modications to the viscosity of the liquids (thickening
liquids), and targeting improved swallowing function
through exercises and maneuvers that compensate
for poor swallowing function or help improve
it.8183,86,137
Pediatric Pulmonology
330 Tutor and Gosa
Anecdotal reports suggest that use of thickeners for
oral liquids may lead to adverse effects in certain pop-
ulations of infants. Clarke and Robinson described the
acute onset of ultimately fatal necrotizing entercolitis
(NEC) in two premature infants who received enteral
feeds thickened with carob bean gum to relieve symp-
toms of GER. They suggested that the use of thickened
feedings may have led to the onset of NEC.137,138 Re-
cently, the US Food and Drug administration warned
that the use of SimplyThick1 should be discontinued in
hospitalized and recently discharged premature infants
after 15 more infants developed NEC and 2 infants
with dysphagia died after using this product to thicken
their feedings. The risk of NEC may be related to the
use of thickening products in general, especially those
made with xanthan gum or other thickeners such as
cornstarch.139 Caregivers may want to consider thicken-
ing liquid feedings with a more natural foodstuff, such
as infant rice cereal, for premature infants with dyspha-
gia, provided the infants are able to digest rice cereal.
Each infants caloric intake, respiratory status, and
gastrointestinal status must also be considered before
making the decision to add rice cereal to the liquid
feedings.
A potential new treatment for dysphagia in the pedi-
atric population is the use of neuromuscular electrical
stimulation to affect the cranial nerves. The stimulation
causes the muscles involved in swallowing to contract,
and this reportedly results in muscle strengthening or
improved motor control. Humbert et al.140 reviewed the
available published evidence regarding the effectiveness
of neuromuscular electrical stimulation as a treatment
for dysphagia. They concluded that it has a potentially
positive effect on recovery from dysphagia, but they
cautioned there is a paucity of available data, lack of
agreement about the effects of it on swallowing func-
tion, and potential for harm with the use of this
modality. Placement of the surface electrodes is
critical, because results opposite to what is desired
have been seen, such as the larynx descending versus
ascending during the swallow.140 Other researchers
have recently reported very little efcacy of neuromus-
cular electrical stimulation for treatment of dysphagia
in children.141,142
GASTROSTOMY/JEJUNOSTOMY TUBE
PLACEMENT FOR SEVERE DYSPHAGIA
Children with dysphagia and chronic aspiration who
continue to have recurrent signicant respiratory symp-
toms despite the use of food modication, positioning,
changes in ow-rate, and utensil use may ultimately
need placement of a temporary or permanent feeding
tube. This may become necessary acutely if there is
inadequate intake of uids or calories to prevent
Pediatric Pulmonology
dehydration or malnutrition. The feeding tube can be
placed nasogastrically or nasojejunally but caregivers
must be adequately trained in the proper insertion of
nasogastric/nasojejunal tubes to prevent their migration
into the lower airway with the resultant signicant risk
of iatrogenic aspiration pneumonia. This approach is
generally used only for short-term treatment. These
types of feeding methods are also used frequently in
critically ill children, to try to reduce the risk of pulmo-
nary aspiration. In a study involving 41 critically ill
children who received transpyloric enteral feedings,
none suffered from pulmonary aspiration and the inci-
dence of pulmonary infection and hepatic dysfunction
diminished during transpyloric enteral feedings. Howev-
er, 10 of the children developed gastrointestinal compli-
cations consisting of abdominal distension, excessive
gastric residual, and diarrhea. Gastrointestinal compli-
cations were more frequent in post-surgical than in
nonsurgical patients.143 Subsequent reports indicate
that the incidence of GER is increased in children
during transpyloric feedings144 and in preterm infants,
the incidence of gastrointestinal disturbances and mor-
tality are increased in those who receive transpyloric
feedings.145
Surgical gastrostomy or jejunostomy tubes may be
placed as an open procedure or by newer laparoscopic
and percutaneous or endoscopic methods.79 Since it is
more difcult to perform a fundoplication after a gas-
trostomy, many surgeons prefer to have an evaluation
done to exclude GER before placement of a gastro-
stomy tube.
Multiple problems can occur after placement of a
gastrostomy tube. The development of granulation tis-
sue around the tube site was the most common problem
sited in two studies occurring in 58% and 68% of
patients, respectively,146,147 followed by tube dislodge-
ment noted in 28% of patients in one of the studies.146
Also, the stoma may close quickly after the tube is
accidently removed making reinsertion difcult if not
impossible without surgical intervention. Other compli-
cations include new or deteriorating GER, infection,
intra-abdominal leakage of feed, and gastrocolic
stulae.148
Both major and minor problems can occur with
placement of a feeding jejuunostomy. In a report
involving 89 patients who underwent placement of the
jejunostomy, 15 patients (15.2%) had complications.
Minor complications (7.2%) included dislodgement,
blockage of the tube, and pericatheter leak. Major com-
plications which required surgical intervention included
detachment of the jejunostomy from the abdominal
wall, leak into the peritoneal cavity, jejunal perforation
by the catheter tip, and peritonitis after removal of the
tube. Procedure related mortality was 3.2%.149 Also,
if the tube is accidently removed, the stoma may close

rapidly making tube reinsertion difcult, if not impossi-
ble, without surgical intervention.
The decision to place a feeding tube either on a tem-
porary or permanent basis has long-reaching implica-
tions in the development of further feeding skills and
the development of social, learning, and emotional
skills.8286
Several studies have been performed over the years
regarding the benet of having an antireux procedure,
such as fundoplication, at the time of placement of a
gastrostomy tube, particularly in children with neuro-
logical impairment. Several studies have reported wors-
ening or de novo development of GER after placement
of a gastrostomy tube alone in 567% of these children.
So far, this has not been predictable by studies such
as pH probe monitoring, biopsy, or radiography. Thus,
534% of children will require anti-GER surgery, such
as fundoplication, to control symptomatic GER.79,150161
Fundoplications can be performed as a complete
(3608) Nissen procedure where the fundus of the stom-
ach is wrapped completely around the esophagus or a
partial procedure, where the fundus is partially wrapped
around the esophagus. Dysphagia, which can be a com-
plication of fundoplication, has reportedly been more
frequent after Nissen versus partial fundoplication in
adults particularly adults with severe esophageal dys-
motility disorders (scleroderma, post-myotomy achala-
sia).162 Partial fundoplication particularly the Toupet
procedure (posterior 2708 wrap of the fundus around
the esophagus) or anterior fundoplication in adults,
may more frequently come unwrapped leading to re-
emergence of GER symptoms.162,163 However, in one
report, 5% of Nissen fundoplications required surgical
revision.163
Performance of a fundoplication can be associated
with several serious intraoperative complications such
as liver laceration, bowel perforation, bleeding, and
peritonitis.164 Other complications include a slipped requirements and reduced use of anticholinergic medi-
or disrupted fundoplication, dehiscence, hiatal hernia,
and bowel obstruction.165 Post-operative development
of dysphagia was noted to be signicantly more severe
after placement of a Nissan fundoplication when com-
pared to placement of a Thal fundoplication in a group
of 175 children.164 Frequent long-term problems have
included gas bloating, dumping syndrome, esophageal
dysmotility, achalasia, inability to vomit or burp, and
slow eating.166 Despite placement of a fundoplication
to reduce GER and placement of a surgical tube for
feeding, some children with dysphagia will continue to
have lower respiratory infections or other signs of aspi-
ration. At that point, one needs to determine if salivary
aspiration is occurring and if so, effective therapy needs
to be provided.
Children who receive tube feedings have signicantly
more oral microora that can be associated with
Dysphagia in Children 331
167
aspiration pneumonia and, they also have more den-
tal plaque and calculus.168 Meticulous oral hygiene/care
and more frequent visits to dentists are recommended
for children who receive tube feedings.167,168 This type
of care has been recommended for critically ill children
to try to help decrease the incidence of ventilator-asso-
ciated pneumonia.169 However, two recent studies did
not demonstrate a decrease in the incidence of ventila-
tor-associated pneumonia in critically ill children who
received tooth brushing or oral hygiene care.170,171 In
children with neurologic impairment and dysphagia,
proper positioning of the head appears to prevent aspi-
ration pneumonias.172
MANAGEMENT OF SALIVARY ASPIRATION
Oral anticholinergic agents, such as glycopyrrolate
or scopolamine patches, have been used, especially
in neurologically impaired children, to treat sialorrhea.
Although effective in decreasing salivation, anticholin-
ergic therapy can be associated with signicant adverse
side effects, including behavioral changes, constipation,
dry mouth, thick secretions, urinary retention, constipa-
tion, ushing, nasal congestion, vomiting, diarrhea, and
tachycardia. Treatment may need to be discontinued in
up to one third of patients.79,173176
In the last few years, several studies have shown that
injections of botulinum toxin, particularly type A, are
effective in controlling sialorrhea in children, particular-
ly those with neurological impairment.177181 The toxin
is usually injected into the submandibular or parotid
salivary glands with sonographic guidance up to four
times per year. Up to 88% of the patients in one study
showed a signicant decrease in saliva production.177
Some researchers also reported a decrease in the num-
bers of hospitalizations and pulmonary infections after
the injections, as well as, reduced pulmonary toilet
cation.178 The reduction in saliva production ranged
from 6 to 28 weeks in one study.179 Reported complica-
tions have included self-limited oral bleeding, viscous
saliva, parotitis, and transient xerostomia in a small
number of patients.177,179,180 Berweck et al.181 reported
a case study of a 15-year-old boy with cerebral palsy
who, after three successful treatment sessions, develop-
ed antibodies to botulinum toxin type B, resulting in
two subsequent treatment sessions with no clinical re-
sponse. In some centers, the use of botulinum toxin has
been discontinued due to migration of the toxin from
the injection site resulting in paralysis of critical bulbar
functions resulting in acute deterioration and death in
children and adults, principally those with amyotrophic
lateral sclerosis (ALS).182 Also, an adult with ALS deve-
loped recurrent jaw dislocation after intraparotid botu-
linum toxin injections for treatment of sialorrhea.183
Pediatric Pulmonology
332 Tutor and Gosa
Surgical management of sialorrhea is an option
in children for whom medical management fails. This
often involves bilateral submandibular and parotid duct
ligation or submandibular gland excision with parotid
duct ligation. Recent studies have reported varying
results, from up to an 87% success rate in controlling
drooling184186 to minimal control of sialorrhea with
surgery.187,188
Children who continue to aspirate and have recurrent
pneumonias despite other medical/surgical therapies
may need the placement of a tracheostomy, particularly
one using a cuffed tracheostomy tube, for pulmonary
toilet. Despite this, there is a lessened but still present
risk of continued aspiration. There is the belief by some
people that a cuffed tracheostomy tube has the potential
of tethering: the larynx which limits its elevation
during swallowing and thus, negatively impacting
swallowing safety.66 As previously mentioned, the use
of a tracheostomy speaking valve has been reported to
reduce but not eliminate occurrences of aspiration,
at least in adults.65 The valve allows movement of air
during exhalation through the vocal cords so that adult
or child with a tracheostomy can speak.
The denitive treatment for the elimination of chron-
ic pulmonary aspiration is LTS or diversion. This proce-
dure eliminates all continuity between the respiratory
and digestive tracts by disconnecting the upper trachea
from the larynx and diverting it directly to a stoma. The
diversion of the proximal trachea to the esophagus
allows for drainage of pooled secretions. With LTS, the
proximal trachea is simply closed, and oral secretions
that accumulate in the larynx are either orally expressed
or swallowed. There is a loss of phonation, and the
patient is left with a permanent tracheostomy.79 Two
recent studies from Japan and one from Brazil docu-
mented the effectiveness of this procedure in children
with intractable aspiration, particularly those who are
neurologically impaired.189191 However, complications
can be considerable, such as tracheal granulations,
bleeding, stenosis of the tracheal stoma, tracheomalacia,
tracheal abscess, ruptured sutures, and tracheocutaneous
stula.189 Even if this procedure is performed without
laryngectomy, LTS may not be reversible.79
CONCLUSION
Due to new advances in technology such as FEES/
FEESST, along with the current standard, VFSS, diag-
nosis of dysphagia, and pulmonary aspiration can now
be made at an early age in children before signicant
morbidity has occurred. Other tests, such as the LLM
index and use of colored dyes may be helpful in diag-
nosing aspiration in limited situations in certain select
children. The salivagram is used to diagnose sialorrhea.
Neuromuscular electrical stimulation therapy could
Pediatric Pulmonology
possibly in the future be a complementary therapy for
children with dysphagia along with the currently avail-
able feeding therapies or use of tube feedings. The use
of botulinum toxin injections and resection of salivary
glands are therapies along with the use of anticholiner-
gic agents and tracheostomy and LTS procedures avail-
able to treat sialorrhea. Infant PFTs have documented
that one of the sequelae of dysphagia and aspiration can
be AO, which should be monitored in symptomatic
infants. Hopefully, all these diagnostic and therapeutic
modalities can help improve the prognosis for many
children with dysphagia or aspiration and decrease
subsequent morbidity and mortality.
ACKNOWLEDGMENTS
We thank Dr. Dennis Stokes and Dr. David Galloway
for their helpful suggestions and critical review of the
manuscript.
REFERENCES
1. Bosma JF. Maturation of function of the oral and pharyngeal
region. Am J Orthod 1963;49:94104.
2. Bosma JF. Oral and pharyngeal development and function. J
Dent Res 1963;42:375380.
3. Bosma JF. Postnatal ontogeny of performance of the pharynx,
larynx, and mouth. Am Rev Respir Dis 1986;13:S10S15.
4. Newman LA. Anatomy and physiology of the infant swallow.
Swallowing and Swallowing Disorders 21;March: 34.
5. Sapienza CM, Ruddy BH, Baker S. Laryngeal structure and
function in the pediatric larynx: clinical applications. Lang
Speech Hear Serv Sch 2004;35:299307.
6. Carr RJ, Beebe DS, Belani KG. The difcult pediatric airway.
Semin Anesth Periop Med Pain 2001;20:219227.
7. Sasaki CT, Levine PA, Laitman JT, Phil M, Crelin ES. Postna-
tal descent of the epiglottis in man: a Preliminary study. Arch
Otolalaryngol Head Neck Surg 1977;103:169171.
8. Sasaki CT, Isaacson G. Functional anatomy of the larynx. Oto-
laryngol Clinic North Am 1988;21:595612.
9. Dodds W. The physiology of swallowing. Dysphagia 1989;
3:171178.
10. Harding R, Johnson P, McClelland ME. Liquid sensitive laryn-
geal receptors in the developing sheep, cat, and monkey. J
Physiol 1978;277:409422.
11. Storey A. A functional analysis of sensory units innervating
epiglottis and larynx. Exp Neurol 1968;20:366383.
12. Storey A. Interaction: of alimentary and upper tract reexes.
In: Sessle AG, editor. Mastication and swallowing. Toronto:
University of Toronto Press; 1976.
13. Karlsson JS, Ambrogio G, Widdicome J. Afferent neural path-
ways in cough and reex bronchoconstriction. J Appl Physiol
1988;65:10071023.
14. Abu-Shweesh JM. Maturation of respiratory reex responses
in the fetus and neonate. Semin Neonatol 2004;9:169180.
15. Seessle B, Lucier G. Functional aspects of the upper respirato-
ry tract and larynx: a review. In: Tilden JT, Roeder LM,
Steinschneider A, editors. Sudden infant death syndrome. New
York: Academic Press; 1983.
16. Gilbert R, Rudd P, Berry PJ, Fleming PJ, Hall E, White DG,
Oreffo PJ, Evans JA. Combined effect of infection and heavy

wrapping on the risk of sudden unexpected infant death. Arch
Dis Child 1992;67:171177.
17. Anas N, Boettrich C, Hall CB, Brooks JG. The association
of apnea and respiratory syncytial virus infections. J Pediatr
1982;101:6568.
18. Pickens DL, Schefft GL, Storch GA, Thach BT. Characteriza-
tion of prolonged apneic episodes associated with respiratory
syncytial virus infection. Pediatr Pulmonol 1989;6:195201.
19. Thach BT. Maturation of cough and other reexes that protect
the fetal and neonatal airway. Pulm Pharmacol Ther 2007;
20:365370.
20. Randolph CD. Gastroesophageal reux and airway disorders.
In: Myers CM III, Cotton RT, Shott SR, editors. The pediatric
airway. An interdisciplinary approach. Philadelphia: JB Lip-
pincott Company; 1995. pp 327357.
21. Dutta S, Matossian H, Meirowitz R, Veeth J. Modulation of
salivary secretion by acid infusion in the distal esophagus in
humans. Gastroenterology 1992;103:18331841.
22. Herbst JJ, Minton SD, Book LS. Gastroesophageal reux caus-
ing respiratory distress and apnea in newborn infants. J Pediatr
1979;95:763768.
23. Boyle J, Tuchman D, Altshuler S, Nixon T, Pack A, Cohen S.
Mechanisms for the association of gastroesophageal reux and
bronchospasm. Am Rev Respir Dis 1985;131:S16.
24. Shaker R, Dodds WJ, Ren J, Hogan WJ, Arndorfer RC. Esoph-
agoglottal closure reex: a mechanism of airway protection.
Gastroenterology 1992;102:857861.
25. Shaker R, Ren J, Hogan WJ, Lin J, Podursan B, Sa Z. Glottal
function during postprandial gastroesophageal reux. Gastoen-
terology 1993;104:A581.
26. Suzuki M, Kirchner JA. Sensory bers in the recurrent laryn-
geal nerve. Ann Otol Rhin Laryngol 1969;78:1.
27. Freiman J, El-Sharkawy TY, Diamant NE. Effect of bilateral
vagosympathetic nerve blockade response of the dog upper
esophageal sphincter (UES) to intraesophageal distention and
acid. Gastroenterology 1981;81:7884.
28. Teabeut RJ. Aspiration of gastric contents. Am J Pathol 1952;
27:5167.
29. Greeneld L, Singleton R, McCaffree D, Coalson J. Pulmo-
nary effects of experimental graded aspiration of hydrochloric
acid. Ann Surg 1969;170:7886.
30. Colombo JL. Pulmonary aspiration. In: Hilman BC, editor. Pe-
diatric respiratory disease: diagnosis and treatment. Philadel-
phia: WB Saunders Company; 1993. pp 429436.
31. Moran T. Experimental aspiration pneumonia. Arch Pathol
1951;52:350354.
32. Hamelburg W, Bosomworth P. Aspiration pneumonitis: experi-
mental studies and clinical observations. Anesth Analg 1964;
43:669676.
33. de Benedictis FM, Carnielli VP, de Benedictis D. Aspiration
lung disease. Pediatr Clin North Am 2009;56:173190.
34. Platzer ACG. Gastroesophageal reux and aspiration syn-
dromes. In: Chernick V, Boat TF, Wilmott RW, Bush A,
editors. Kendigs disorders of the respiratory tract in children,
7th edition. Philadelphia: Saunders El Sevier; 2006. pp 592
609.
35. Amaizu N, Shulman RJ, Schanler RJ, Lau C. Maturation of
oral feeding skills in preterm infants. Acta Paediatr 2008;97:
6167.
36. Gewolb IH, Vice FL, Schweitzer-Kenney EL, Taciak VL. De-
velopmental patterns of rhythmic suck and swallow in preterm
infants. Dev Med Child Neurol 2001;43:2227.
37. Lau C, Smith EO, Schanler RJ. Coordination of suck-swallow
and swallow respiration in preterm infants. Acta Paediatr
2003;92:721727.
Dysphagia in Children 333
38. Gewolb IH, Bosma JF, Taciak VL, Vice FL. Abnormal devel-
opmental patterns of suck and swallow rhythms during feeding
in preterm infants with bronchopulmonary dysplasia. Dev Med
Child Neurol 2001;43:454459.
39. Gewolb IH, Bosnia JF, Reynolds EW, Vice FL. Integration of
suck and swallow rhythms during feeding in preterm infants
with and without bronchopulmonary dysplasia. Dev Med Child
Neurol 2003;45:344348.
40. Gewolb IH, Vice FL. Abnormalities in the coordination of res-
piration and swallow in preterm infants with bronchopulmo-
nary dysplasia. Dev Med Child Neurol 2006;48:595599.
41. Sheikh S, Allen E, Shell R, Hrushak J, Iram D, Castile R,
McCoy K. Chronic aspiration without gastroesophageal reux
as a cause of chronic respiratory symptoms in neurologically
normal infants. Chest 2001;120:11901195.
42. Taubenhaus LJ. Bottle propping for infant feeding. J Pediatr
1968;72:669672.
43. Khoshoo V, Ross G, Kelly B, Edell D, Brown S. Benets of
thickened feeds in previously healthy infants with respiratory
syncytial virus bronchiolitis. Pediatr Pulmonol 2001;31:301
302.
44. Haddad J Jr. Congenital disorders of the nose. In: Kliegman
RM, Behrman RE, Jenson HB, Stanton BF, editors. Nelson
textbook of pediatrics, 18th edition. Philadelphia: Saunders El
Sevier; 2001. p 1743.
45. Khafagy YW. Endoscopic repair of bilateral congenital choa-
nal atresia. Laryngoscope 2002;112:316319.
46. Samad DS, Shah UK, Handler SD. Choanal atresia: a twenty-
year review of medical comorbidities and surgical outcomes.
Laryngoscope 2003;113:254258.
47. Orenstein S, Peters J, Khan S, Youssef N, Hussain SZ. Con-
genital anomalies: esophageal atresia and tracheoesophageal
stula. In: Kliegman RM, Behrman RE, Jenson HB, Stanton
BF, editors. Nelson textbook of pediatrics, 18th edition. Phila-
delphia: Saunders El Sevier; 2007. pp 15431544.
48. Tinanoff N. Syndromes with oral manifestations. In: Kliegman
RM, Behrman RE, Jenson HB, Stanton BF, editors. Nelson
textbook of pediatrics, 18th edition. Philadelphia: Saunders El
Sevier; 2007. pp 15331534.
49. Parhizkar N, Saltzman B, Grote K, Starr J, Cunningham M,
Perkins J, Sie K. Nasopharyngeal airway management of
airway obstruction in infants with micrognathia. Cleft Palate
Craniofac J 2010;48:478482.
50. Kirschner RE, Low DW, Randall P, Bartlett SP, McDonald-
McGinn DM, Schultz PJ, Zackai EH, LaRossa D. Surgical air-
way management in Pierre Robin sequence: is there a role for
tongue-lip adhesion? Cleft Palate Craniofac J 2003;40:1318.
51. Denny AD, Amm CA, Schefer RB. Outcomes of tongue-lip
adhesion for neonatal respiratory distress caused by Pierre
Robin sequence. J Craniofac Surg 2004;15:819823.
52. Cruz MJ, Kerschner JE, Beste DJ, Conley SF. Pierre Robin
sequences: secondary respiratory difculties and intrinsic feed-
ing abnormalities. Laryngoscope 1999;109:16321636.
53. Cozzi F, Totonelli G, Frediania S, Zani A, Spagnol L, Cozzi
DA. The effect of glossopexy on weight velocity in infants
with Pierre Robin syndrome. J Pediatr Surg 2008;43:296298.
54. Denny AD, Amin C. New technique for airway correction in
neonates with severe Pierre Robin sequence. J Pediatr 2005;
147:97101.
55. Wells TR, Landing BH, Shamszadeh M, Thompson JW, Bove
KE, Caron KH. Association of Down syndrome and segmental
tracheal stenosis with ring trachea cartilages: a review of nine
cases. Pediatr Pathol 1992;12:673682.
56. Su W, Berry M, Puligandia PS, Aspirot A, Flageole H,
Laberge JM. Predictors of gastroesophageal reux in neonates
Pediatric Pulmonology
334 Tutor and Gosa
with congenital diaphragmatic hernia. J Pediatr Surg 2007;
42:16391643.
57. Peetsold MG, Kneepkens CM, Heij HA, IJsselstijn H, Tibboel
D, Gemke RJ. Congenital diaphragmatic hernia: long-term risk
of gastroesophageal reux disease. J Pediatr Gastroenterol
Nutr 2010;51:448453.
58. Guner YS, Elliott S, Marr CC, Greenholz SK. Anterior fundo-
plication at the time of congenital diaphragmatic hernia repair.
Pediatr Surg Int 2009;25:715718.
59. Chamond C, Morineau M, Gouizi G, Bargy F, Beaudoin S.
Preventive antireux surgery in patients with congenital dia-
phragmatic hernia. World J Surg 2008;32:24542458.
60. Andrews TM, Myer CM III, Bailey WW, Vester SR. Intratho-
racic lesions involving the tracheobronchial tree. In: Myer CM
II, Cotton RT, Shott SR, editors. The pediatric airway: an inter-
disciplinary approach. Philadelphia: JB Lippincott Company;
1995. pp 223245.
61. Rotschild A, Dison PJ, Chitayat D, Slimano A. Mid-facial
hypoplasia associated with long-term intubation for broncho-
pulmonary dysplasia. Am J Dis Child 1990;144:13021306.
62. Eibling DE, Gross RD. Subglottic air pressure. A key compo-
nent of swallowing efciency. Ann Otol Rhinol Laryngol
1996;105:253258.
63. Gross RD, Mahlmann J, Grayhack JP. Physiologic effects of
open and closed tracheostomy tube on the pharyngeal swallow.
Ann Otol Rhinol Laryngol 2003;112:143152.
64. Abraham SS, Wolf EL. Swallowing physiology of toddlers
with long-term tracheostomies. A Preliminary study. Dyspha-
gia 2000;15:206212.
65. Elpern EH, Borkgren OM, Bacon M, Gerstung C, Skrzynski
M. Effects of the Passy-Muir tracheostomy speaking valve on
pulmonary aspiration in adults. Heart Lung 2000;29:287293.
66. Lim JW, Lerner PK, Rothstein SG. Epiglottic position after
cricothroidotomy: a comparison with tracheostomy. Ann Otol
Rhinol Laryngol 1997;106:560562.
67. Leigh JM, Maynard JP. Pressure on the tracheal mucosa from
cuffed tubes. Br Med J 1979;5:11731174.
68. Geha AS, Seegers JV, Kodner IJ, Lefrak S. Tracheoesophageal
stula caused by cuffed tracheal tube. Successful treatment by
tracheal resection and primary repair with four-year follow-up.
Arch Surg 1978;113:338340.
69. Matsumoto M, Kawakami Y, Naitoh H, Higashi T, Kohno K,
Uchida H, Kurasako T, Takatori M, Tada K. Massive hemor-
rhage induced by trachea-innominate artery stula in two
infants. Masui 1991;40:807811.
70. Arena JM. Hydrocarbon poisoningcurrent management.
Pediatr Ann 1987;16:879883.
71. Bysani GK, Rucoba RJ, Noah ZL. Treatment of hydrocarbon
pneumonitis. Chest 1994;106:200203.
72. Gurwitz D, Kattan M, Lvison IT, Culham JAG. Pulmonary
function abnormalities in asymptomatic children after hydro-
carbon pneumonitis. Pediatrics 1978;62:789794.
73. Colombo JL, Thomas HM. Aspiration syndromes. In: Taussig
LM, Landau LI, Lesouef PN, Morgan WJ, Martinez FD, Sly
PD, editors. Pediatric respiratory medicine, 2nd edition. Phila-
delphia: Mosby El Sevier; 2008. pp 337345.
74. Colombo JL, Halberg TK. Airway reactivity following repeat-
ed milk aspiration in rabbits. Pediatr Pulmonol 2000;29:113
119.
75. Janahi IA, Elidemir O, Shardonofsky FR, Abu-Hassan MN,
Fann LL, Larsen GL, Blachburn MR, Colaurdo GN. Recurrent
milk aspiration produces changes in airway mechanics, lung
eosinophils, and goblet cell hyperplasia in a murine model.
Pediatr Res 2000;48:776781.
Pediatric Pulmonology
76. Harding SM. Gastroesophageal reux: a potential asthma trig-
ger. Immunol Clin North Am 2005;25:131148.
77. Lefton-Greif MA, Carroll JL, Loughlin GM. Long-term fol-
low-up of oropharyngeal dysplasia in children without appar-
ent risk factors. Pediatr Pulmonol 2006;41:10401048.
78. Colombo JL. Chronic recurrent aspiration. In: Kliegman RM,
Behrman RE, Johnson HB, Stanton BF, editors. Nelson text-
book of pediatrics, 18th edition. Philadelphia: Saunders El
Sevier; 2007. pp 17901792.
79. Boesch RP, Daines C, Wilging JP, Kaul A, Cohen AP, Wood
RE, Amin RS. Advances in the diagnosis and management of
chronic pulmonary aspiration in children. Eur Respir J 2006;
28:847861.
80. Zanetti G, Murchior E, Gasparetto TD, Escaissato DL, Soaresa
SA Jr. Lipoid pneumonia in children following aspiration of
mineral oil used in the treatment of constipation: high resolu-
tion CT ndings in 17 patients. Pediatr Radiol 2007;37:1135
1139.
81. Kramer SS, Eicher PM. The evaluation of pediatric feeding
abnormalities. Dysphagia 1993;8:215224.
82. Newman LA. Optimal care patterns in pediatric patients with
dysphagia. Semin Speech Lang 2000;21:281291.
83. Lefton-Greif MA. Pediatric dysphagia. Phys Med Rehabil Clin
N Am 2008;19:837851.
84. De Pippo KL, Holas MA, Reding MJ. Validation of the 3-
ounce water swallow test for aspiration. Arch Neurol 1992;49:
12591261.
85. Suiter DM, Leder SB, Karas DB. The 3-ounce (90-cc) water
swallow challenge: a screening test for children with suspected
oropharyngeal dysphagia. Otolaryngol Head Neck Surg 2009;
140:187190.
86. Lefton-Greif MA, McGrath-Morrow SA. Deglutition and respi-
ration: development, coordination, and practical implications.
Semin Speech Lang 2007;28:166179.
87. Tabee A, Johnson PE, Gartner CJ, Kalwerisky K, Desloge RB,
Stewart MG. Patient-controlled comparison of endoscopic
evaluation of swallowing with sensory testing (FEESST) and
videouoroscopy. Laryngoscope 2006;116:821825.
88. Rao N, Brady SL, Chadhuri G, Donzelli JJ, Wesling MW.
Gold standard? Analysis of the videouroscopic and beroptic
endoscopic swallow examinations. J Appl Res 2003;31:ss1.
89. Langmore SE, Schatz K, Olson N. Endoscopic and videouro-
scopic evaluations of swallowing and aspiration. Ann Otol
Rhinol Laryngol 1991;100:678681.
90. Perie S, Laccourreye L, Flahault A, Hazebroucq V, Chaussade
S, St Gully JL. Role of videoendoscopy in assessment of
pharyngeal function in oropharyngeal dysphagia: comparison
with videouroscopy and manometry. Laryngoscope 1998;108:
17121716.
91. Leder SB, Karas DE. Fiberoptic endoscopic evaluation of
swallowing in the pediatric population. Laryngoscope 2000;
110:11321136.
92. da Silva AP, Lubianca Neto JF, Santoro PP. Comparison be-
tween videouroscopy and endoscopic evaluation of swallow-
ing for the diagnosis of dysphagia in children. Otolaryng Head
Neck Surg 2010;143:204209.
93. Wilging JP. Endoscopic evaluation of swallowing in the pediat-
ric population. Int J Pediatr Otorhinolaryngol 1995;32:S107
S108.
94. Arvedson J, Rogers B, Buck G, Smart P. Silent aspiration
prominent in children with dysphagia. Int J Pediatr Otorhino-
laryngol 1994;28:173181.
95. Taniguchi MH, Moyer R. Assessment of risk factors for pneu-
monia in dysphagic children: signicance of videouoroscopic

swallowing evaluation. Dev Med Child Neurol 1994;36:495
502.
96. Hiorns MO, Ryan MM. Current practice in paediatric video-
uroscopy. Pediatr Radiol 2006;36:911919.
97. Benson J, Lefton-Greif MA. Videouroscopy of swallowing in
pediatric patients: a component of the total feeding evaluation.
In: Tichman DN, Walter RS, editors. Diagnosis of feeding and
swallowing in infants and children: pathophysiology, diagno-
sis, and treatment, 1st edition. San Diego: Singular Publishing
Group; 1994. pp 187200.
98. Arvedson JC. Assessment of pediatric dysphagia and feeding
disorders: clinical and instrumental approaches. Dev Disabil
Res Rev 2008;14:118127.
99. Rees CJ. Flexible endoscopic evaluation of swallowing with
sensory testing. Curr Opin Otolaryngol Head Neck Surg 2006;
14:425430.
100. Aviv JE, Kim T, Sacco RL, Kaplan S, Goodhart K, Diamond
B, Close LG. FEESST: a new bedside endoscopic test of the
motor and sensory components of swallowing. Ann Otol Rhi-
nol Laryngol 1998;107:378387.
101. Aviv JE, Kim T, Thomson JE, Sunshine S, Kaplan S, Close
LG. Fiberoptic endoscopic evaluation of swallowing with sen-
sory testing (FEESST) in healthy controls. Dysphagia 1998;
13:8792.
102. Aviv JE, Kaplan ST, Thomson JE, Spitzer J, Diamond B, Close
LG. The safety of exible endoscopic evaluation of swallow-
ing with sensory testing (FEESST): an analysis of 500 conse-
cutive evaluations. Dysphagia 2000;15:3944.
103. Aviv JE, Murry T, Zschommler A, Cohen M, Gartner C. Flexi-
ble endoscopic evaluation of swallowing with sensory testing:
patient characteristics and analysis of safety in 1,340 consecu-
tive examinations. Ann Otol Rhinol Laryngol 2005;114:173
176.
104. Wilging JG, Thompson DM. Pediatric FEESST: beroptic en-
doscopic evaluation of swallowing with sensory testing. Curr
Gastroenterol Rep 2005;7:240243.
105. Colombo JL, Halberg TH. Recurrent aspiration in children:
lipid-laden macrophage index. Pediatr Pulmonol 1987;3:
8689.
106. Furuya ME, Moreno-Cordova V, Ramirez-Figueroa JL, Vargas
MH. Cutoff value of lipid-laden alveolar macrophages for di-
agnosing aspiration in infants and children. Pediatr Pulmonol
2007;42:452457.
107. Bauer ML, Lyrene RK. Chronic aspiration in children. Evalua-
tion of the lipid-laden macrophage index. Pediatr Pulmonol
1999;28:7982.
108. Knauer-Fisher S, Ratjen F. Lipid-laden macrophages in bron-
choalveolar lavage as a marker for pulmonary aspiration.
Pediatr Pulmonol 1999;27:419422.
109. Kazachkov MY, Muhlbach MS, Livasy CA, Noah TC. Lipid-
laden macrophage index and inammation in bronchoalveolar
lavage uids in children. Eur Respir J 2001;18:790795.
110. Kajetaowicz A, Stinson D, Laybolt KS, Resch L. Lipid-laden
macrophages in the tracheal aspirate of neonates receiving
intralipids: a pilot study. Pediatr Pulmonol 1999;28:101
108.
111. Wang JY, Kuo PH, Jan IS, Lee LN, Yang PC. Serial analysis
of fat-containing macrophages in bronchoalveolar lavage uid
in a patient with fat embolism. J Formos Med Assoc 2001;
100:557560.
112. Wright BA, Jeffrey PH. Lipoid pneumonia. Semin Respir In-
fect 1990;5:314321.
113. Ding Y, Simpson PM, Schekkhase DE, Tryka AF, Ding L, Par-
ham DM. Limited reliability of lipid-laden macrophage index
restricts its use as a test for pulmonary aspiration comparison
Dysphagia in Children 335
with a simple quantitative assay. Pediatr Dev Pathol 2002;
5:551558.
114. Colombo JL, Halberg TK, Samut PH. Time course of lipid-
laden pulmonary macrophages with acute and recurrent milk
aspiration in rabbits. Pediatr Pulmonol 1992;12:9598.
115. Ahrens P, Noll C, Kitz R, Willigens P, Zielen S, Hofman D.
Lipid-laden macrophages (LLAM); a useful marker of silent
aspiration in children. Pediatr Pulmonol 1999;28:8388.
116. Heyman S, Respondek M. Detection of pulmonary aspiration
in children by radionuclide salivagram. J Nucl Med 1989;30:
697699.
117. Bar-Sever Z, Connolly LP, Treves ST. The radionuclide saliva-
gram in children with pulmonary disease, a high risk of aspira-
tion. Pediatr Radiol 1995;25:S180S183.
118. Levin E, Colon A, DiPalma J, Fitzpatrick S. Using the radio-
nuclide salivagram to detect pulmonary aspiration and esoph-
ageal dysmotility. Clin Nucl Med 1993;18:110114.
119. Baikie G, South MJ, Reddihough DS, Cook DJ, Cameron DJ,
Olinsky A, Ferguson E. Agreement of aspiration tests using
barium videouroscopy, salivagram, and milk scan in children
with cerebral palsy. Dev Med Child Neurol 2005;47:8693.
120. Cook SP, Lawless S, Mandell GA, Reilly JS. The use of the
salivagram in the evaluation of severe and chronic aspiration.
Int J Petiatr Otorhinolaryngol 1997;41:353361.
121. Finder JD, Yellon R, Charron M. Successful management of
tracheostomized patients with chronic saliva aspiration by use
of constant positive airway pressure. Pediatrics 2001;107:
13431345.
122. Amanntea SL, Piva JP, Sanches PR, Palombini BC. Oropha-
ryngeal aspiration in pediatric patients with endotracheal intu-
bation. Pediatr Crit Care Med 2004;5:152156.
123. Brady SL, Hildner CD, Hutchins BF. Simultaneous videouo-
scopic swallow study and modied Evans blue dye procedure:
an evaluation of blue dye visualization in cases of known aspi-
ration. Dysphagia 1999;14:146149.
124. Peruzzi WT, Logeman JA, Currie D, Moen SG. Assessment of
aspiration in patients with tracheostomies comparison of bed-
side colored dye assessment with videouroscopic examina-
tion. Respir Care 2001;46:243247.
125. Donzelli J, Brady S, Wesling M, Craney M. Simultaneous
modied Evans blue dye procedure and videonasal endoscopic
evaluation of the swallow. Laryngoscope 2002;111:17461750.
126. ONeil-Pirzzi TM, Lisiecki DJ, Jack MK, Connors JJ, Milliner
MP. Simultaneous modied barium swallow and blue dye
tests: a determination of the accuracy of blue dye test aspira-
tion ndings. Dysphagia 2003;18:3238.
127. Belafsky PC, Blumenfeld L, LePage A, Nahrstedt K. The ac-
curacy of the modied Evans blue dye test in predicting aspi-
ration. Laryngoscope 2003;113:19691972.
128. Winklmaier U, Wust K, Plinkert PK, Wallner F. The accuracy
of the modied Evans blue dye test in detecting aspiration in
head and neck cancer patients. Eur Arch Otorhinolaryngol
2007;264:10591064.
129. Abraham S, Wolf E. Swallowing physiology of toddlers with
long term trcheostomies: a preliminary study. Dysphagia 2000;
15:206212.
130. Rosingh H, Peek S. Swallowing and speech in infants follow-
ing tracheostomy. Acta Oto-rhino-laryngologica 1999;53:
5963.
131. Leder S, Baker K, Goodman R. Dysphagia testing and aspira-
tion status in medically stable infants requiring mechanical
ventilation via tracheotomy. Pediatr Crit Care Med
2010;11:484487.
132. Norman C, Louw B, Kritzinger A. Incidence and description
of dysphagia in infants and toddlers with tracheostomies: a
Pediatric Pulmonology
336 Tutor and Gosa
retrospective review. Int J Pediatr Otorhinolaryngol 2007;
71:10871092.
133. Lucarelli MR, Shirk MB, Julian MW, Crouser ED. Toxicity of
food drug and cosmetic blue no. 1 dye in critically ill patients.
Chest 2004;125:793795.
134. Tutor J, Srinivasan S, Gosa M, Culbreath B, Mallory L, Redd
L, Jones M, Curry R, Davis Christensen M, Schoumacher R,
Stokes D. Pulmonary function in infants with chronic aspira-
tion. Am J Respir Crit Care Med 2010;181:A6229.
135. Turner SJ, Stick SM, LeSouef KL, Sly PD, LeSouef PN. A
new technique to generate and assess forced expiration from
raised lung volume in infants. Am J Respir Crit Care Med
1995;151:14411450.
136. ATS/ERS task force on standards for infant respiratory func-
tion test. ATS/ERS statement: raised volume forced expiration
in infants. Am J Respir Crit Care Med 2005;172:14631471.
137. Gosa MM, Schooling T, Coleman J. Thickened liquids as
a treatment for children with dysphagia and associated
adverse effects: a systematic review. ICAN 2011; doi:10.117/
1941406411407664.
138. Clarke P, Robinson M. Thickening milk feeds may cause nec-
rotizing entercolitis. Brit Med J 2004;89:F280.
139. Abrams SA. Be cautious in using thickening agents for pre-
emies. AAP News, American Academy of Pediatrics, 2011
[Epub].
140. Humbert IA, Poletto CJ, Saxon KG, Kearney PR, Crujido L,
Wright-Harp W, Payne J, Jeffries N, Sonies BC, Ludlow LL.
The effect of surface electrical stimulation on hypolaryngeal
movement in normal individuals at rest and during swallowing.
J Appl physiol. 2006;101:16571663
141. Clark H, Lazarus C, Arvedson J, Schooling T, Frymark T.
Evidence-based systemic review; Effects of neuromuscular
electrical stimulation on swallowing and neural activation. Am
J Speech Lang Pathol 2009;18:361375.
142. Christiaanse ME, Mabe B, Russell G, Smeone TL, Fortnato J,
Rubin B. Neuromuscular electrical stimulation is no more ef-
fective than usual care for the treatment of primary dysphagia
in children. Pediatr Pulmonol 2011;46:559565.
143. Panadero E, Lopez-Herce J, Caro L, Sanchez A, Cueto E,
Bustinza A, Moral R, Carrilo A, Sanco L. Transpyloric enteral
feeding in critically ill children. J Pediatr Gastroenterol Nutr
1998;26:4348.
144. Rosen R, Hart K, Warlaumont M. Incidence of gastroesopha-
geal reux during transpyloric feeds. J Gastroenterol Nutr
2011;52:532535.
145. McGuire W, McEwan P. Systematic review of transpyloric
versus gastric tube feeding for preterm infants. Arch Dis Child
Fetal Neonatal Ed 2004;89:F245F248.
146. Naiditch JA, Lautz T, Barsness KA. Postoperative complica-
tions in children undergoing gastrostomy tube placement. J
Laparoendosc Adv Surg Tech A 2010;20:781785.
147. Goldberg e, Barton S, Xanthopoulos MS, Stettler N, Liacouras
CA. A descriptive study of complications of gastrostomy tube
in children. J Pediatr Nurs 2010;25:7280.
148. Petters RT, Balduyck B, Nour S. Gastrostomy complications
in infants and children: a comparative study. Pediatr Surg Int
2010;26:707709.
149. Kaushik SP. Technical complications of feeding jejunostomy: a
critical analysis. Trop Gastroenterol 1997;18:127128.
150. Mollitt DL, Golladay ES, Seibert JJ. Symptomatic gastro-
esophageal reux following gastrostomy in neurologically
impaired patients. Pediatrics 1985;75:11241126.
151. Jolley SG, Smith EL, Tunell WP. Protective antireux opera-
tion with feeding gastrostomy. Experience with children. Ann
Surg 1985;201:736740.
Pediatric Pulmonology
152. Langer JC, Wesson DE, Ein SH, Filler RM, Shandling B,
Superina RA, Papa M. Feeding gastrostomy in neurologically
impaired children: is an antireux procedure necessary? J
Pediatr Gastroenterol Nutr 1988;7:837841.
153. Wheatley MJ, Wesley JR, Tkach DM, Coran AG. Long-term
follow-up of brain-damaged children requiring feeding gastro-
stomy: should antireux procedure be performed? J Pediatr
Surg 1991;26:301305.
154. Heine RG, Reddihough DS, Catto-Smith AG. Gatroesophageal
reux and feeding problems after gastrostomy in children with
severe neurological impairment. Dev Med Child Neurol 1995;
37:320329.
155. Ish JA, Recorla FJ, Scherer LR III, West KW, Groseld JL.
The development of gastroesophageal reux after percutaneous
gastrostomy. J Pediatr Surg 1997;32:321322.
156. Sulaeman E, Udall JN Jr, Brown RF, Manick EE, Loe WA,
Hill CB, Schmidt-Sommerfeld E. Gastroesophageal reux and
Nissen fundoplication following percutaneous endoscopic gas-
trostomy in children. J Pediatr Gastroentrol Nutr 1998;26:269
273.
157. Puntis JW, Thwaites R, Abel G, Stringer MD. Children with
neurological disorders so not need fundoplication concomitant
with percutaneous endoscopic gastrostomy. Dev Med Child
Neurol 2000;42:9799.
158. Hament JM, Box NM, van der Zee DC, Schryver JE, Nesselaar
C. Complications of percutaneous endoscopic gastrostomy
with or without concomitant antireux surgery in 96 children.
J Pediatr Surg 2001;36:14121415.
159. Burd RS, Price MR, Whalen TV. The role of protective antire-
ux procedures in neurologically impaired children: a decision
analysis. J Pediatr Surg 2002;237:500506.
160. Novtny NM, Jester AL, Ladd AP. Preoperative prediction of
need for fundoplication before gastrostomy tube placement in
children. J Pediatr Surg 2009;44:173176.
161. Srivastava R, Downey EC, OGorman M, Feola P, Samore M,
Holubkov R, Munorff M, James BC, Rosenbaum P, Young PC,
Dean JM. Impact of fundoplication versus gastrojejunal feed-
ing tubes on mortality and in preventing aspiration pneumonia
in young children with neurological impairment who have gas-
troesophageal reux disease. Pediatrics 2009;123:338345.
162. Limpert PA, Naunheim KS. Partial versus complete fundopli-
cation: is there a correct answer? Surg Clin North Am 2005;
85:399410.
163. Baigrie RJ, Cullis SN, Ndhluni AJ, Cariem A. Randomized
double-blind trial of laparoscopic Nissen fundoplication versus
anterior partial fundoplication. Br J Surg 2005;92:819823.
164. Kubiak R, Andrews J, Grant HW. Laporascopic Nissen fundo-
plication versus Thal fundoplication in children: comparison of
short-term outcomes. J Laparoendosc Adv Surg Tech A 2010;
20:665669.
165. Ashcraft KW, Holder TM, Armoury RA. Treatment of gastro-
esophageal reux in children by Thal fundoplication. J Thorac
Cardiovasc Surg 1981;82:706712.
166. DiLorenzo C, Orenstein S. Fundoplication friend or foe? J
Pediatr Gastroenterol Nutr 2002;34:117124.
167. Jawadi AH, Cassamassimo PS, Griffen A, Enrile B, Marcone
M. Comparison of oral ndings in special needs children with
and without gastrostomy. Pediatr Dent 2004;26:283288.
168. Dement HA, Casas MJ. Dental care for children fed by tube: a
critical review. Spec Care Dentist 1999;19:220224.
169. Johnstone L, Spense D, Koziol-McClain J. Oral hygiene care
in the pediatric intensive care unit: practice recommendations.
Pediatr Nurs 2010;36:8596.
170. Ames NJ. Evidence to support tooth brushing in critically ill
patients. Am J Crit Care 2011;20:242250.

171. Jacomo AD, Carmona F, Matsuno AK, Manso PH, Carlotti
AP. Effect of oral hygiene with 0.12% chlorhexidine gluconate
on the incidence of nosocomial pneumonia in children under-
going cardiac surgery. Infect Control Hosp Epidemiol 2011;
32:591596.
172. Van den Engel-Hoek L, Erasmus CE, van Bruggen HW,
de Swart BJ, Sie LT, Steenks MH, de Groot IJ. Dysphagia in
spinal muscular atrophy type II: more than a bulbar problem?
Neurology 2009;73:17871791.
173. Bachrach SJ, Walter RS, Tzcinski K. Use of glycopyrrolate
and other anticholingeric medications for sialorrhea in children
with cerebral palsy. Clin Pediatr 1998;37:485490.
174. Mier RJ, Bachrach SJ, Lakin RC, Barker T, Childs T, Moran
M. Treatment of sialorrhea with glycopyrrolate: a double-blind
dose-ranging study. Arch Pediatr Adolesc Med 2000;154:
12141218.
175. Blasco PA, Stansbury JC. Glcopyrrolate treatment of chronic
drooling. Arch Pediatr Adolesc Med 1996;150:932935.
176. Stern LM. Preliminary study of glycopyrrolate in the manage-
ment of drooling. J Pediatr Child Health 1997;33:5254.
177. Pena AH, Cahill AM, Gonzalez L, Baskin KM, Towbin RB.
Botulinum toxin A injection of salivary glands in children with
drooling and chronic aspiration. J Vasc Inter Radiol 2009;
20:368373.
178. Raval TH, Elliott CA. Botulinum toxin injection to the salivary
glands for the treatment of sialorrhea with chronic aspiration.
Ann Otol Rhinol Laryngol 2008;117:118122.
179. Krause E, Botzel K, de la Chaux R, Gurkov R. Local botu-
linum toxin A for treating chronic sialorrhea. HNO 2008;56:
941946.
180. Wilken B, Aslamai B, Backes H. Successful treatment of
drooling in children with neurological disorders with botu-
linum toxin A or B. Neuropediatrics 2008;39:200204.
181. Berweck S, Schroeder AS, Less SH, Bigalke H, Heinen F. Sec-
ondary non-response due to antibody formation in a child after
injections of botulinum toxin B into the salivary glands. Dev
Med Child Neurol 2007;49:6264.
Dysphagia in Children 337
182. Meijer JW, van Kujik AA, Geurts AC, Schelhaas HJ, Zwarts
MJ. Acute deterioration of bulbar function after botulinum tox-
in treatment for sialorrhea in amyotrophic lateral sclerosis. Am
J Med Rehabil 2008;87:321324.
183. Tan EK, Lo YL, Seah A, Auchus AP. Recurrent jaw
dislocation after botulinum toxin treatment for sialorrhea
in amyotrophic lateral sclerosis. J Neurol Sci 2001;190:
9597.
184. Manrique D, do Brasil OO, Ramos H. Drooling: analysis and
evaluation of 31 children who underwent bilateral submandib-
ular gland excision and parotid duct ligation. J Otorhinolar-
yngol 2007;73:4044.
185. Greensmith AL, Johnstone BR, Reid SM, Hazard CJ, Johnson
HM, Reddihugh DS. Prospective analysis of the outcome of
surgical management of drooling in the pediatric population: a
10-year experience. Plas Reconstr Surg 2005;116:1233
1242.
186. Crysdale WS, McCann C, Roske L, Joseph M, Semenuk D,
Chait P. Saliva control issues in the neurologically challenged.
A 30 year experience in team management. INT J Pediatr
Otorhinolaryngol 2006;70:519527.
187. Stamataki S, Behar P, Brodsky L. Surgical management of
drooling: clinical and caregiver satisfaction outcomes. In t J
Pediatr Otorhinolaryngol 2008;72:18011805.
188. Martin TJ, Conley SF. Long-term efcacy of intra-oral surgery
for sialorrhea. Otorhinolaryngol Head Neck Surg 2007;137:
5458.
189. Miyamoto A, Kitahuta A, Fukuda I, Oka R, Cho K, Tanaka H.
Surgical management for intractable aspiration in handicapped
children. No To Hattatsu 2009;41:2731.
190. Manrique D, Settanni FA, Compones de Brasil OO. Surgery
for aspiration: analysis of laryngotracheal separation in 23
children. Dysphagia 2006;21:254258.
191. Takamizawa S, Tsugawa C, Nishijima E, Muraji T, Satoh S.
Laryngotracheal separation for intractable aspiration pneumo-
nia in neurologically impaired children: experience with 11
cases. J Pediatr Surg 2003;38:975977.
Pediatric Pulmonology