Recurrent or chronic
pulmonary aspiration (CPA) describes the recurrent passage of food,
gastric contents, or saliva into the airway, resulting in symptoms
such as cough, wheeze, choking, pneumonia, or lung damage.35-40 CPA
may occur only sporadically in some children, when other stressors,
such as upper respiratory tract infections, are also present. Often,
more than 1 mechanism of CPA is present, complicating diagnosis
and management. Because it is known that small amounts of saliva
and gastric contents may be aspirated in normal individuals1,2,
it is often difficult to determine if CPA is causing lung disease.
The 3 main mechanisms of CPA are (1) swallowing dysfunction resulting in
the direct aspiration of food, (2) GER and aspiration, and (3) failure
to protect the airway from oral secretions, resulting in the aspiration
of saliva and oral contents. These mechanisms are discussed separately
in terms of their pathophysiology, clinical features, diagnosis,
and treatment. Complications and outcomes are addressed globally.
to Swallowing Dysfunction
Normal swallowing is a complex activity that involves a multitude of
voluntary and involuntary actions. It can be divided into 3 phases.
In the oral phase, food is mixed with saliva and ground to an appropriately
sized bolus by the voluntary action of mastication. The tongue must
compress the bolus against the hard palate to cause the bolus to
pass into the oropharynx. In the pharyngeal phase, the tongue opposes
the palate and the soft palate opposes the pharynx to prevent regurgitation
of the bolus into the mouth or nose. The larynx elevates and the
glottis closes at both the false and true cords to prevent aspiration
of the bolus into the airway. The pharyngeal constrictors then contract
sequentially and reflexively to propel the bolus into the esophagus.
At the cricopharyngeus muscle, there is a short relaxation of the
upper esophageal sphincter, due to elevation of the larynx, that
allows the bolus to be passed into the esophagus. The subsequent
contraction of the cricopharyngeus muscle then serves to propel
the bolus into the esophagus, starting the esophageal phase. In
this phase, the peristalsis continues down the esophagus, reaching
the lower esophageal sphincter. This sphincter relaxes about 2 seconds after
the initiation of swallowing and stays relaxed for 8 to 10 seconds.
Once the peristaltic wave reaches it, it also contracts and returns
to its natural tone after 10 to 15 seconds. Any abnormality in the
complex sequence of events can result in aspiration. Swallowing
dysfunction occurs most frequently in individuals with neurologic
disorders or any of the predisposing factors listed in Table 511-1, but it should be considered
in any child with suspicious symptoms.
and Clinical Manifestations
Typical symptoms of aspiration
due to swallowing dysfunction include coughing, wheezing, choking, and
gagging that is temporally related to the intake of food. It may
be intermittent, occurring only at times of stress such as during
upper respiratory tract infections; it may be positional, and it
often changes over time with growth and development. Unfortunately,
direct aspiration of food can also be silent, especially in neurologically
compromised children, so it is important to have a high index of
suspicion. Repeated bouts of direct aspiration can lead to significant
morbidity from recurrent bronchitis or pneumonia and bronchiectasis
as well as chronic hypoxia and dyspnea. Left untreated, children
can die from respiratory failure.
The pathophysiology of lung damage arises from the inflammatory
cascade triggered by the aspiration. Levels of interleukin-8 and
tumor necrosis factor-α are increased, and there
is a significant neutrophilic migration to the site of aspiration
with subsequent activation and sequestration of the neutrophils.
This leads to epithelial damage, increased permeability, decreased
compliance, and, over time, scarring.41 There is
no difference in the extent of neutrophilic infiltration between
acidic (from stomach acid) and neutral (direct aspiration) aspirated
The approach to the evaluation and treatment of children with swallowing
dysfunction is discussed in detail in Chapter 31.
Aspiration of Gastroesophageal Reflux
GER occurs occasionally in almost everyone when food mixed with
gastric contents moves in a retrograde manner from the stomach through
the lower esophageal sphincter into the esophagus. It is common
in infants under a year old, but it is rarely pathologically symptomatic
(see also Chapter 394). It is also common,
often pathologically, in the individuals listed in Table 511-1. Anything that reduces lower esophageal
sphincter tension, such as medication, tubes, and anatomic lesions,
increases the likelihood of GER. Even direct feeding into the stomach
via gastrostomy, especially at night, increases the likelihood of
and Clinical Manifestations
Acid is irritating and induces inflammation in the
airway.3,18 Even aspiration of materials
with a pH higher than 2.5 induces pneumonitis in an animal model.75 This
would indicate that when aspiration of gastric contents occurs regularly,
pulmonary disease ensues. There is evidence that GER is associated
with respiratory symptoms such as cough, wheeze, pneumonia, and
apnea.76-78 There is also evidence
of an association of GER with lung disease, documented by improvement
in pulmonary symptoms with treatment of GER.78 A
causal relation between GER and respiratory symptoms due to aspiration
is much more difficult to prove.79-81 We know that
stimulation of esophageal receptors by GER can cause reflex bronchospasm, cough,
and wheeze without actual aspiration of GER.82 Two
small studies in adults simultaneously measured pH in the esophagus
and the trachea to prove a temporal relation between drop in pH
in the esophagus and drop in pH in the trachea and respiratory symptoms,
including decreased peak flow measurements.83,84 One
documented that laryngeal exposure to acid decreases the sensation
of the larynx, diminishing its ability to defend against aspiration,
so chronic GER without aspiration may eventually lead to GER with
aspiration.85 Our challenge is to
determine when GER is pathological and when aspiration in occurring.
The gold standard for diagnosing GER has been 24-hour esophageal pH
monitoring. The upper gastrointestinal series or barium esophagram
has also been a test to determine the presence of GER. Neither of
these tests determines aspiration. Flexible bronchoscopy with bronchoalveolar
lavage or gastroesophageal scintigraphy are often also necessary.
or Impedance Monitoring
pH monitoring is considered the gold standard for detecting GER.
Most studies are done with 2 pH channels, one just above the lower
esophageal sphincter and the other in the posterior pharynx. It
detects drops in pH, indicating the presence of acid from the stomach
at those 2 levels. Done over 24 hours, it is a reasonable test of
GER of acid. It cannot, however, detect nonacid reflux or acid reflux
events that occur after a pH drop but before pH normalization. Because
of its limitations, it must be performed in individuals who are
not on acid suppressive medication.86,87
Multichannel intraluminal impedance
with pH monitoring (MII-pH) is a newer technique that has certain
advantages of traditional pH monitoring. It can measure the change
in electrical impedance along the length of the esophagus. It can
track the movement of gas or liquid boluses, both anterograde and
retrograde; detect both acid and nonacid liquid boluses; determine
if the bolus is being swallowed or refluxed; and determine how high
along the esophagus the bolus moves.88 It
is better able than pH monitoring to detect pharyngeal-level reflux,89-91 and
in one study in infants, it detected a large number of events that
correlated with respiratory symptoms on sleep study, only 12% of
which were acid.89 Unfortunately,
MII-pH is not yet widely available due to startup costs and technical
support for the procedure.
Both studies will diagnose GER, but neither study,
even with pharyngeal channels, can detect aspiration. These studies
must be used in conjunction with direct evidence of aspiration.
simple test detects the presence of reflux of swallowed barium.
Its advantages are that it is simple, inexpensive, and quick. It
also detects certain anatomic lesions such as vascular rings and
malrotation. Unfortunately, it captures GER only if GER happens
to occur during the study, and it cannot quantify GER. Once again,
it can detect GER, not aspiration, and must be used in conjunction
with direct evidence of aspiration.
with Bronchoalveolar Lavage
As mentioned previously, the use of LLMI obtained during
bronchoscopy is used most often as evidence of aspiration due to
GER. Finding lipid, however, in the lower airways does not help determine
whether the lipid came from GER or from direct aspiration due to
swallowing dysfunction. Using alternative markers of GER aspiration
is a topic of significant research. In recent years, pepsin has
been studied and found to have good correlation with respiratory
symptoms when found in the airways.92-95 Having
a marker specific to GER versus food would help distinguish between
direct aspiration and aspiration of GER. Currently, bronchoscopy
results must be used together with other evidence of GER, absence
of swallowing issues and clinical findings to formally diagnose
aspiration of GER.
has been used as a physiologic means of determining aspiration of
GER.96 Technetium Tc99 is mixed with a child’s
milk or food and the child is allowed to eat. Serial radiologic images
are then captured to detect tracer in the lungs. Unfortunately, this
test does not clearly distinguish between aspiration from swallowing
and aspiration from GER. It also seems to have a low sensitivity.96-99 In
one study, positive scans were found in only 6% of children
with cerebral palsy, a group of children who have a much higher
prevalence of aspiration, based on VSS and salivagrams. This test,
however, is much less invasive than bronchoscopy and does not require a
great deal of radiation, allowing multiple uses if necessary. In
children with a gastrostomy, it can distinguish between GER and swallowing
dysfunction if the radiotracer is given via tube.
In the case of aspiration of GER, dye studies are only helpful
if the child has a gastrostomy or jejunostomy and a tracheostomy
tube. Dye can be mixed with tube feedings and detected with tracheal suctioning.
If aspiration is seen, it is accurate and helpful. If not, it may
be falsely negative.
of GER is the first line of treatment. This includes the use of
thickened feeds, which has been shown to decrease nonacid reflux
events by MII-pH.100 Pharmaceuticals
include histamine blockers, such as ranitidine and famotidine, and
proton pump inhibitors, such as omeprazole. Acid blockade makes
gastric contents more neutral, decreasing their toxicity to the
airway if aspirated, but it does not prevent aspiration of GER.
Prokinetic agents are also used, but choices in the United States
are limited, and effectiveness is questionable. Metoclopramide has
not had widely proven efficacy and has side effects that may limit
its use.101 Erythromycin is also used,
at both antimicrobial and low-dose options mainly in infants, with
mixed results but without significant side effects.102-105 It
has had some efficacy on antral gastric motility.106 Domperidone
is available as a promotility agent outside of the United States,
but it also has not been demonstrated to be clearly effective against
GER.107 No pharmacological agents
have been tested specifically against aspiration.
For children who have failed
medical therapy, fundoplication is the surgical option of choice.
Generally, fundoplications are successful with good outcomes, but
surgical complications are still possible. When fundoplications
are too tight, they can impede movement of food, liquid, and saliva
into the stomach, leaving it in the distal esophagus and increasing
the likelihood of aspiration. Improvement of pulmonary symptoms
with fundoplication occurs in 48% to 92% of children.108-111 Recurrence
of GER occurs in approximately 10%, but in most cases,
repeat fundoplication can be performed successfully.110â115 Children
with neurologic disorders have a higher rate of failure of fundoplication,
approximately 25%.108,110,112 These
are the same children who are at higher risk for from aspiration,
so reevaluation for GER is warranted if symptoms persist. Evaluation
for complicating pathology, including dysmotility and eosinophilic
esophagitis, should be performed before fundoplication because these
children are most likely to have complications such as retching
and failure to improve from surgery.
children who have failed fundoplication, or who have contraindications
to fundoplication, another option is feedings into the jejunum.116,117 Placement
of a surgical jejunostomy will allow for full feeds with reduced
risk of GER and aspiration. Aspiration of gastric secretions is
still possible. If temporary feeding into the jejunum is necessary,
placement of a nasojejunal tube or gastrojejunal tube is possible,
but these tubes obstruct the pylorus and/or lower esophageal sphincter,
impeding passage through these openings. They are also prone to
displacement, requiring radiologically guided replacement. All jejunal
feedings must be done as a continuous drip, and jejunal tubes carry
the risk of inducing intussusception.
A final option in extreme cases where other options have all
failed is esophagogastric separation with permanent gastrostomy
tube for feeding and esophageal drainage into the jejunum.118,119 Unfortunately,
even with this procedure, there seem to be complications because
a high number of these children appear to mishandle their oral secretions,
aspirating these instead of gastric contents.
Aspiration of saliva is the most insidious type of aspiration.
Some nocturnal aspiration of saliva can occur in healthy individuals,2 so
understanding when aspiration of saliva is pathological is key to prevention
of complications. Recognizing symptoms and having a high index of
suspicion, especially in high-risk children (Table
511-1), will help prevent poor outcomes.
and Clinical Manifestations
The clinical symptoms of aspiration of oral secretions include choking
and gagging as well as chronic or intermittent cough and wheeze
and recurrent pneumonia. Additionally, these children often have
sialorrhea with drooling and pooling of saliva in the mouth. They
often have overt choking on their saliva and may improve when positioned
so saliva runs out of the mouth. Many of these children are developmentally
delayed, although cranial nerve palsies, vocal cord paralysis, laryngoesophageal
cleft, and craniofacial abnormalities also lead to inability to
handle saliva appropriately. In these children, their swallowing
is severely dysfunctional, not allowing them to swallow saliva appropriately,
and their laryngeal sensation is abnormal, not allowing them to
protect their airway adequately.120 Saliva contains
bacteria and yeast that are potentially pathological to the lungs
if aspirated in large enough quantities or frequently. Recurrent
pneumonia or even pulmonary abscesses are possible.31 Aspiration
of oral secretions, not inflammation due to food or gastric acid,
is the main source of lung damage. Unfortunately, children who aspirate
oral secretions are likely to also aspirate food and to have pathologic
GER. Evaluation for salivary aspiration may need to occur simultaneously
with evaluation for other types of aspiration.
In children with suspected aspiration and either treated or absent GER,
who are being fed parenterally, these diagnostic tests are essential.
In children with potentially confounding causes of aspiration, these
tests may be necessary or should be performed concomitantly with
others to rule out other forms of aspiration.
This test is often considered the gold standard
for detection of salivary aspiration. Its accuracy, however, has
not been evaluated. Similar to gastroesophageal scintigraphy, this
test involves using a small amount of radiotracer placed on the
tongue, in the buccal pouch or as a continuous infusion.121,122 Subsequent
detection in the lower airways or lungs can diagnose aspiration
of the oral secretions. The test is usually readily available and often
used because of its simplicity, noninvasive nature, nonreliance
on oral feeding, and low radiation exposure.
Studies have shown positive salivagrams in 26% to
28% of children suspected of aspirating oral secretion,
but none of these studies had any confirmatory tests, most being
done prior to use of FEES.123-125 This
test also has poor agreement with VSS and milk scan,99 but
it has been used successfully in one case to titrate nocturnal tracheal
positive pressure.126 There is no
doubt that the salivagram can detect salivary aspiration. It appears,
however, that many children who might, at least intermittently,
aspirate their saliva are missed with this test.
Fees with Sensory
previously, FEES allows direct visualization of the larynx with
observation of the swallowing mechanism without feeding. Pooling
of secretions and penetration or aspiration of oral secretions can
be seen with a small amount of dye added to the secretions. Sensory
testing involves graduated puffs of air delivered to the larynx
to determine the threshold necessary to induce protective laryngeal
reflexes and can help distinguish those at risk for aspiration.
There is good evidence that this testing can predict the tendency
toward aspiration without giving the child a feeding.46,127-130
In assessing salivary aspiration in a child with a tracheostomy,
dye is placed on a child’s tongue and detected by suctioning
stained secretions from the tracheostomy. Its sensitivities and
specificities are similar to those when dye is mixed with oral or
tube feedings; if aspiration is seen, it is accurate, but false
negatives occur regularly.
first line of therapy for aspiration of saliva is pharmacological to
reduce salivary flow. Some studies have evaluated behavioral modification
to control drooling, with positive results, but none of these actually
decrease salivary flow.131,132 Salivary
flow reduction can be accomplished by anticholinergics. Glycopyrrolate
administered orally at a dose of 0.04 to 0.1 mg/kg/dose
will reduce saliva but may have diminishing effects, the longer
a child takes it.133 Glycopyrrolate
is also associated with anticholinergic side effects such as flushing,
urinary retention, constipation, behavior changes, and mucus plugging
that may make some children stop taking it.133-135 Mucus
plugging is the most concerning because it may cause respiratory
distress or even be life threatening. Using antihistamines such
as cetirizine for drooling has had anecdotal success. Scopolamine
patches tend to be more successful than antihistamines, with few
side effects.136,137 Because treatment
is usually accomplished with a patch, titration can be difficult.
Generally, a single patch is applied every 72 hours, although partial
patches have also been tried. No studies have shown that medical
treatment actually prevents aspiration or resultant lung damage
even though it reduces salivary flow.
injection into the salivary glands can paralyze the glands and reduce
saliva production. All studies of this therapy have demonstrated
improvement of sialorrhea, but length of response varies.138-140 There
does seem to be a need for repeat therapy as the toxin wears off;
no long-term studies of efficacy of repeated doses have been done.
There has not been any study of the impact of botulinum toxin injection
on aspiration or lung disease.
Surgical options include ligation of salivary ducts or removal
of certain salivary glands. This therapy can serve to permanently
decrease salivary flow. Ligation of the ducts of the parotid and
submandibular glands or excision of the submandibular glands and
ligation of the parotid ducts has been used with good success in
children.141-144 Two studies have also shown a
reduction in hospitalizations and lower respiratory tract infections in
children who have undergone the procedures.141,143 Prospective
studies and comparisons with other techniques such as botulinum
injection still need to be assessed.
Another option is insertion of a tracheostomy tube. This alone does
not decrease salivation and cannot prevent aspiration. It does allow
for suctioning of aspirated saliva to hopefully prevent pneumonia. Some
children who aspirate saliva require tracheostomy for upper airway
obstruction and other reasons. There is evidence that swallowing
is affected in children with tracheostomy,145,146 which
may make children more prone to aspiration. If a child is placed
on positive pressure ventilation, aspiration may be less likely
because of the positive pressure in the lower airway impeding passive
influx of saliva.
The definitive treatment for salivary aspiration is physical
separation of the upper airway from the lower airway.147-150 This
is accomplished by a separation of the larynx from the trachea with
the trachea diverted to a permanent stoma. A complete laryngectomy
may also be performed. This surgery will prevent aspiration of saliva and
may allow for oral feedings, but it will prevent phonationand may
not be reversible. It should be considered in children with intractable
aspiration who are experiencing progressive lung damage or life-threatening pneumonias.
of Recurrent Aspiration
Radiographic testing is not diagnostic of recurrent pulmonary
aspiration and cannot distinguish among the types of aspiration.
It can, however, give evidence of pulmonary inflammation or damage
and help us to assess the pulmonary impact of the aspiration.
radiographs from children who aspirate are nonspecific. They may
show peribronchial thickening, atelectasis, scattered infiltrates,
or hyperinflation. In advanced cases, bronchiectasis may also be
present. Radiographs obtained during acute aspiration pneumonia
are more likely to show active disease with segmental or lobar infiltrate,
especially in dependent areas of the lung (Fig.
A chest radiograph from a neurologically devastated child
who presented with respiratory failure, fever, and wheezing. He
chronically aspirates his oral secretions, and this episode began
with upper respiratory symptoms. An endotracheal tube that is too
low has been placed. The patchy infiltrates are most prominent in
Computed Tomography of the Chest
computed tomography (HRCT) scanning gives more precise information about
lung damage than do plain radiographs (Fig. 511-2).
These scans demonstrate the detail of bronchiectasis, “tree-in-bud” opacities,
and air trapping more clearly.151-153 These
findings are often seen in children who aspirate, especially in
dependent portions of the lung. Findings may be present before clinical
symptoms of chronic lung disease are present, so obtaining an HRCT
should be considered in most children with potential CPA. Any single
HRCT is a single point in time. Serial HRCT can follow progression
or resolution of lung damage with time and interventions. High-resolution
technique is preferred because it provides more detail.
High-resolution computed tomography scans in the same
patient in 2002 (top) and 2003. The patient had esophageal atresia
at birth treated with colonic interposition. She was a chronic aspirator
of refluxed food. Tree-in-bud opacities, bronchial wall thickening,
air trapping, and linear densities are all seen and most prominent
in the right upper lobe. Bronchiectasis progressed from 2002 to
2003 because the child continued to aspirate.
Acute Small Volume Aspiration
in large-volume aspirations, small-volume aspirations of gastric
material and food, although irritating, are sterile and do not require
antibiotics. Aspiration must be treated acutely
when symptoms are present. As in large-volume aspirations, small-volume
aspirations of gastric material and food, although irritating, are
sterile and do not require antibiotics. The children may require
supportive care, such as suctioning, oxygen, or bronchodilators,
to treat bronchospasm for hours to days after the event. These aspirations
may be witnessed and involve vomiting or choking on food. Close
monitoring is warranted to ensure a secondary bacterial infection
does not occur, especially in children with bronchiectasis or tracheostomies or
with other risk factors, who may have lower airway colonization with
bacteria (Table 511-2).
Aspiration of oral contents may, instead, result in aspiration
pneumonia from aspiration of pathogenic bacteria from the upper airway. These
may include anaerobes, common mouth flora, or secretions from the
nose, ears, and sinuses containing common upper respiratory pathogens. Children with
true aspiration pneumonia may have fever, persistent cough, and
wheeze in addition to acute respiratory distress. Treatment should
be supportive, as described previously, but also should include antibiotics
to cover common upper respiratory pathogens (Table
of Recurrent Aspiration
long-term complications of aspiration include chronic disabling
symptoms associated with airway inflammation such as chronic cough
and wheeze. Recurrent bacterial pneumonias occur in the inflamed
airway that has altered host defenses. Pneumonias can lead to lung
damage and bronchiectasis. Bronchiectasis manifests as dilated, chronically
inflamed airways characterized by impaired mucus clearance. Subsequent
infections in these airways lead to pulmonary fibrosis and scarring
with respiratory insufficiency. The ultimate complication is death
from overwhelming aspiration pneumonia. Potential complications
from therapy include inadequate nutritional intake and malnutrition,
intolerance to tube feeds, or worsening of GER with subsequent aspiration. Growth
and development must be carefully monitored in children who cannot
consume all calories orally. Medications and surgeries also have
potential complications, so no therapy should be instituted without
considering the risks versus the benefits, as well as the impact
on the child’s quality of life.
Outcomes are dependent on the successful, early institution of therapy.
If aspiration of food, liquid, and saliva is prevented, the symptoms
of airway inflammation and lung damage can also be prevented. Airway
inflammation is reversible, and some bronchiectasis may also be
reversible, significantly reducing the morbidity and mortality. Alternatively, when
aspiration is allowed to continue, the outcome is usually progressive
lung damage, respiratory insufficiency and disability (chronic oxygen
dependency), and occasionally death from overwhelming pneumonia.