Abstract
The presence and significance of aspiration is a common consideration for children seen in “aerodigestive centers.” Aspiration, the passage of food or liquid below the larynx, can be acute or chronic. Chronic repeated aspiration provides challenges to the clinician for both diagnosis and treatment. Children with chronic medical problems and certain syndromes are at increased risk of dysphagia and aspiration, although aspiration is occasionally seen in otherwise healthy children. This chapter describes the etiologies of swallowing dysfunction, common diagnostic tools to evaluate the causes of swallowing dysfunction, and specific considerations in special populations. The multidisciplinary evaluation of dysphagia and lung injury caused by chronic repeated aspiration is also described.
Keywords
chronic pulmonary aspiration, dysphagia, aerodigestive
Introduction
Aspiration refers to the penetration of material below the subglottic area and into the lower airways. There are two main aspiration syndromes: (1) an acute aspiration event quickly progressing to acute pneumonitis and possibly respiratory failure, and (2) chronic repeated aspiration of very small volumes that leads to a persistent smoldering inflammatory state and eventually results in chronic lung injury. Acute aspiration of a large volume of gastric contents or even small volumes of hydrocarbon-containing liquids induces a severe toxic injury to airway mucosa with mucosal edema, bronchorrhea, and airway obstruction. Injury to terminal respiratory units causes pulmonary edema and an acute respiratory distress syndrome (ARDS)-like presentation that may be life-threatening. Injury to terminal respiratory units is more common with hydrocarbon aspiration as the volatile liquid produces a vapor that is subsequently inhaled deeper into the lungs; long-term pulmonary fibrosis may follow hydrocarbon aspiration. Nonvolatile lipid-containing liquids (e.g., mineral oil) are not absorbable, and aspiration results in persistent lipoid pneumonia, bronchiolar obstruction, and chronic lung injury. For lipoid pneumonia, repeated bronchoalveolar lavage (BAL) may be both diagnostic and therapeutic.
Chronic pulmonary aspiration is a common problem in pediatrics and remains a diagnostic and therapeutic challenge. Chronic aspiration is almost always a consideration in the evaluation of the “aerodigestive” patient and therefore will be the focus of the remainder of this chapter.
Chronic pulmonary aspiration represents the repeated passage of food material, gastric refluxate, or saliva into the subglottic airways in sufficient quantities to cause chronic or recurrent respiratory symptoms. Aspiration results from failure of the airway protection that occurs in the setting of repeated opportunities for aspiration to occur. These opportunities may be nearly continuous, such as with severe hypopharyngeal pooling of oral secretions, or intermittent, such as with reflux of gastric contents above the upper esophageal sphincter or with swallowing dysfunction. Aspiration may be limited to specific consistencies, such as during swallowing of thin liquids. In general, aspiration is the result of one or more of the following: anatomic abnormalities within the aerodigestive tract, disruptions of the complex neurologic sensorimotor networks of swallowing and respiration, or functional disorders of the esophagus or muscles of deglutition ( Fig. 76.1 ).
Chronic aspiration is very common in aerodigestive patients, as they generally present with complicated underlying medical conditions, including feeding failure, gastroesophageal reflux (GER), neurologic injury, chronic respiratory disease, tracheostomy, impaired laryngeal function, and airway lesions resulting in obstructed breathing, or abnormal connections between the airway and gastrointestinal tract. Aspiration is more common in patients with certain congenital syndromes or in those born very prematurely. Because of their complex multisystem disorders, it may be difficult to distinguish between the symptoms of other underlying conditions (e.g., bronchopulmonary dysplasia or tracheobronchomalacia) and chronic aspiration. The symptoms of chronic aspiration are common to many respiratory conditions, and a reliance on symptoms of dysphagia and recurrent pneumonias will fail to identify many children with significant chronic lung injury from aspiration. The most common symptoms of chronic aspiration include: chronic cough, wheezing, congestion, choking or gagging with feeds, failure to thrive, apnea, intermittent fever spikes, and recurrent chest infections. The parental report of “wet vocal quality” or “wet breathing” may be the most predictive symptoms of aspiration.
Chronic pulmonary aspiration can result in significant morbidity. Children may be hospitalized for recurrent pneumonias and commonly develop progressive lung injury and bronchiectasis. Significant bronchiectasis may persist into adulthood and result eventually in respiratory failure. Chronic pulmonary aspiration is the leading cause of death in neurologically impaired patients and those with congenital syndromes such as Cornelia de Lange and Cri du Chat. Some children, particularly those without neurologic injury, are diagnosed inappropriately as having asthma and may develop irreversible lung injury before chronic aspiration is suspected, identified, and treated. The histopathology of chronic aspiration is that of bronchiolocentric organizing pneumonia with giant cells and granuloma formation; the gold standard diagnosis is identification of vegetable matter ( Fig. 76.2 ). This correlates with findings of bronchiolar obstruction and injury seen on high-resolution computed tomography (CT) of the chest: centrilobular (“tree-in-bud”) opacities, and bronchiectasis. In animal models of chronic aspiration, repeated aspiration of small food particles results in the greatest injury as a chronic foreign body reaction causes damage to the architecture of the lung parenchyma. In mouse models of a single small aspiration event, the inflammatory response to small food particles is amplified by acidification of the aspirated material.
Aspiration Caused by Swallowing Dysfunction
Normal swallowing is a complex process that is dependent upon intact anatomy and well-organized sensory and motor function of specific cranial and cervical nerves. The oral phase is voluntary and includes acceptance and preparation of the food bolus, which includes sucking or chewing and manipulating a bolus on the tongue. The bolus is usually delivered to the pharynx in voluntary fashion, but premature spillage of material into the hypopharynx can occur if oral movements are not coordinated. Once bolus delivery occurs, the involuntary pharyngeal phase is triggered and airway protection takes place. This is a sequential event involving cessation of respiration, adduction of the true vocal folds in association with horizontal approximation of the arytenoid cartilages, closure of the false vocal folds, and retroversion of the epiglottis. The combination of elevation of the larynx and contraction of intrinsic laryngeal muscles allows the epiglottis to serve as a gutter, diverting food and liquids laterally into the pyriform sinus region. The larynx is elevated under the base of the tongue, facilitating the stretching and opening of the cricopharyngeus, as the pharyngeal constrictors shorten the pharynx and propel the bolus through the upper esophageal sphincter. Once passage of the bolus occurs, the larynx returns to its resting position and the airway reopens. The bolus is subsequently transported to the stomach by peristalsis, aided by gravity. Protection against aspiration is provided by the functional anatomy of swallowing and by protective reflexes; any breakdown in the structure, effectiveness, or coordination of these components may result in failure of safe swallowing. A more complete description of the swallowing process and mechanisms of aspiration during swallowing can be found in Chapter 77 .
Development of Swallowing
Development of swallowing begins early in fetal life, and the aerodigestive tract development is integrated with that of the respiratory centers of the brainstem. Central pattern generation in the brainstem controls and coordinates movements of mastication, respiration, and deglutition through adaptive networks of interneurons densely bundled within the nucleus ambiguus and nucleus tractus solitarius. Ultrasound studies have demonstrated pharyngeal swallowing as early as 10 to 14 weeks gestation, nonnutritive sucking and swallowing at 15 weeks, and sucking with anterior to posterior tongue movements between 18 and 24 weeks gestation. At 26 to 29 weeks gestation, reflexes between taste buds and facial muscles can be demonstrated, and nonnutritive sucking on a pacifier may be observed. Some infants can feed by mouth at 32 to 33 weeks, although 34 weeks is the earliest that infants can sustain full nutrition and hydration orally. At 34 weeks, sucking becomes more rhythmic and organized. Beyond term, swallowing matures, characterized by increased sucking and swallowing rates, longer sucking bursts, and larger volumes per suck. At 3 to 4 months of age, lateral tongue movements aid in bolus formation, allowing children to eat pureed consistency from a spoon by 6 months of age.
Swallowing Dysfunction in Specific Populations
Chronic pulmonary aspiration secondary to swallowing dysfunction most often occurs secondary to central or peripheral neurologic disease, functional immaturity, or anatomic limitations ( Box 76.1 ). While most children who aspirate have some combination of these factors, there are children who have swallowing dysfunction (usually delayed initiation of swallowing) with aspiration sufficient to cause chronic respiratory symptoms and lung injury without any identifiable anatomic, neurologic, or developmental limitations. These children may require gastrostomy tube placement, but generally the swallowing dysfunction resolves between 2 and 3 years of age.
Prematurity
Congenital anatomic abnormalities
Esophageal atresia
Tracheoesophageal fistula
Laryngotracheoesophageal cleft
Choanal stenosis or atresia
Cleft palate
Macroglossia
Laryngomalacia
Micrognathia
Vascular ring
Tracheal stenosis
Cystic hygroma
Laryngeal/pharyngeal vascular malformation
Acquired anatomic abnormalities
Laryngeal/pharyngeal tumors
Laryngeal/pharyngeal trauma
Tracheostomy
Congenital syndromes
CHARGE association
Möbius
Pfeiffer
Cornelia de Lange
Cri du chat
Down syndrome
Gastrointestinal
Esophageal dysmotility
Esophageal foreign body
Cricopharyngeal achalasia
Gastroesophageal reflux
Central nervous system
Depressed consciousness
Static or progressive encephalopathy
Traumatic brain injury
Cerebrovascular accident
Hydrocephalus
Peripheral neurologic
Arnold Chiari malformation
Vocal cord paralysis
Neurologic-variant laryngomalacia
Neuromuscular
Muscular dystrophy
Myotonic dystrophy
Spinal muscle atrophy
Myasthenia gravis
Guillain-Barré syndrome
Otherwise normal child with isolated aspiration
The newborn infant and especially the preterm infant are particularly susceptible to aspiration caused by tenuous coordination between sucking, swallowing, and breathing. Children and adults typically initiate swallowing during the mid-expiratory phase, with an obligatory deglutition apnea, followed by further expiration to help prevent aspiration of residual liquid. Term infants younger than 6 months of age will most often swallow at the very end of inspiration and the onset of expiration. Premature infants have more varied phase relationships due to variable rates of development of coordination between central deglutition and respiration. Fatigue of the swallowing mechanism can also develop toward the end of a prolonged feeding session, especially in infants with respiratory disease and increased work of breathing.
Chronic aspiration is highly prevalent in children with neurologic impairment, such as static encephalopathy and neuromuscular disorders. Children with neurologic impairment frequently require prolonged feeding times. Choking with feeding, chest infections, and dysphagia may be present in nearly all children with severe cerebral palsy. Aspiration may occur before, during, or after a swallow and often does not provoke cough clearance. Common mechanisms include poor oral preparation, neck extension impairing laryngeal elevation, premature spillage of liquids, poor pharyngeal clearance with excessive residual, and poor esophageal opening. Aspiration is the most common cause of death in these patients. Children with Down syndrome are at increased risk for aspiration, and an instrumental evaluation of swallowing is indicated in all infants with marked hypotonia, slow feeding or choking, persistent respiratory symptoms, and unexplained failure to thrive. This population may have anatomic, neurologic, and functional abnormalities that place them at high risk of aspiration. The prevalence of feeding disorders is also very high in children and adolescents with inherited neuromuscular disorders, such as spinal muscle atrophy, Duchenne muscular dystrophy, and myotonic muscular dystrophy. While some diseases have specific contributing characteristics (e.g., macroglossia in Duchenne muscular dystrophy), nearly all are associated with prolonged transit time, poor laryngeal elevation, decreased pharyngeal squeeze, and persistent pharyngeal residual related to neuromuscular weakness. These patients are particularly subject to fatigue with prolonged oral feeding.
Peripheral neurologic diseases and injury can result in chronic pulmonary aspiration. Vocal cord paralysis (bilateral more than unilateral), which may result from a difficult delivery or surgery within the mediastinum, may interfere with coordination of respiration and swallowing and impair protective posterior glottic closure. Congenital syndromes that result in lower cranial nerve dysfunction, such as Möbius syndrome or CHARGE association (coloboma, heart defect, atresia choanae, retarded growth and development, genital hypoplasia, and ear anomalies), are frequently complicated by chronic aspiration. Among children with CHARGE association, dysphagia and aspiration are as common as most of the major associations. Similarly, dysphagia with vocal cord dysfunction, pharyngoesophageal dysmotility, and aspiration can be a presenting feature of Arnold-Chiari malformations due to compression of the brainstem and the subsequent effect on lower cranial nerve function. Cricopharyngeal achalasia may be associated with Arnold-Chiari malformation but also may be an independent congenital cause for aspiration. Cricopharyngeal achalasia creates opportunities for aspiration due to delayed passage of food bolus into the esophagus and increased pooling of food and oral secretions in the hypopharynx.
Anatomic abnormalities anywhere along the aerodigestive tract may impact deglutition and result in increased risk for chronic aspiration. Children with craniofacial malformations (e.g., choanal stenosis and cleft palate) are susceptible to chronic aspiration caused by decreased coordination of swallowing and breathing. Crowding of the pharyngeal airway caused by macroglossia or retrognathia creates risks for aspiration. Neck cysts and tumors may narrow and distort the upper aerodigestive tract as well as impair the movements of laryngeal and pharyngeal structures of deglutition. These include cystic hygromas, lymphatic malformations, neuroblastomas, and hemangiomata. The upper airway anatomy also can be distorted by caustic ingestion, thermal inhalational injury, or trauma. Lingual and palatine tonsil hypertrophy also may be associated with aspiration, particularly in neurologically impaired patients, and treatment may improve dysphagia. Any lesion resulting in persistent or intermittent upper airway obstruction can disrupt the timing of the swallow. Laryngomalacia is the best recognized of these causes, as feeding problems are the second most common presenting symptom after stridor. In children with laryngomalacia caused by tight aryepiglottic folds or tall prolapsing arytenoids, surgical treatment can effectively improve both stridor and aspiration. Supraglottoplasty should be considered cautiously, however, in patients with apparent laryngomalacia caused by poor upper airway tone (i.e., “neurologic-variant laryngomalacia”), as aspiration may be worsened following surgery in these patients.
Anatomic abnormalities, such as congenital esophageal atresia with tracheoesophageal fistula (EA/TEF) and laryngotracheoesophageal cleft (LTEC), also result in aspiration during swallowing, though not due to abnormalities in deglutition. These cause direct connections between the esophagus and the airway. EA/TEF is typically detected at birth and repaired. Even after repair, children with EA/TEF often continue to aspirate. The dysphagia associated with repaired EA/TEF is multifactorial and due to not only abnormal esophageal motility and gastroesophageal reflux but also abnormalities of the tracheal wall including tracheomalacia. Oropharyngeal dysphagia and oral aversion are also seen in children with repaired EA/TEF with or without associated congenital anomalies. Aspiration of thin liquids drunk quickly is the typical history for a LTEC. H-type TEF and LTEC are difficult to detect, and diligent investigation by a skilled rigid bronchoscopist is generally required. Even mild LTEC (types 1 and 2) may be associated with significant symptoms (e.g., stridor, feeding problems, recurrent respiratory infections), even when radiographic swallowing studies do not demonstrate frank aspiration ( 
and 
).
Children with tracheostomy tubes are at increased risk for chronic pulmonary aspiration due to their underlying medical conditions as well as the presence of the tracheostomy. The presence of a tracheostomy tube affects many important components of swallowing: impaired laryngeal elevation, alterations in timing, and prevention of the rise in subglottic pressure. While an association between impaired swallowing and the presence of a tracheostomy tube has been documented, there is no study that demonstrates the development of de novo aspiration following tracheostomy placement in children. Children with tracheostomies who chronically aspirate may benefit from the use of a one-way speaking valve when anatomically appropriate. This restores physiologic positive end expiratory pressure (PEEP) and allows subglottic pressure to elevate with swallowing. This can also be achieved with positive pressure applied to the tracheostomy tube by continuous positive airway pressure (CPAP) or a ventilator.
Evaluation of Swallowing
Swallowing function can be evaluated by clinical examination by a trained speech and language pathologist, by radiographic investigation, or endoscopically. Each method has strengths and weaknesses. Clinical evaluations by trained providers provide excellent assessment of feeding behaviors, aversions, and oral motor skills. They can screen for possible aspiration but cannot evaluate silent symptoms. One study reported a negative predictive value of 89% for aspiration of liquids, yet the reported positive predictive value was worse: 54% for liquids and 18% for solids. When the clinical exam suggests aspiration, an instrumental evaluation of swallowing, either radiographic or endoscopic, should be performed to confirm it. Thorough descriptions of radiographic videofluoroscopic swallow studies (also known as modified barium swallows) and fiberoptic endoscopic evaluation of swallowing (FEES; 
and 
), which can directly evaluate the oral, pharyngeal, and esophageal phases of swallowing, are reviewed in Chapter 77 . Generally, a videofluoroscopic swallow (VSS) study is a standard evaluation for direct aspiration (“from above”) for children in whom clinical evaluation has suggested abnormal swallowing.
Role of Radiographic and Endoscopic Tests in the Evaluation of Aspiration
Radiographic swallow studies and FEES are both valuable tools for the evaluation of deglutition, but they have unique strengths and weaknesses ( Table 76.1 ). They are equally sensitive in their abilities to detect delayed initiation of swallow, penetration, aspiration, and postswallow residue. A prospective, randomized trial in dysphagic adults found no differences in pneumonia outcomes whether feeding recommendations were made based on FEES or videofluoroscopic swallow study results. The sensitivity of radiographic swallow studies can be improved by studying many swallows, especially as this may bring out the effects of fatigue. However, radiographic assessment of the child who has not been orally feeding (because of prolonged illness or oral aversions) is very limited. FEES is useful in these situations, as aspiration risk can be evaluated by assessing vocal cord function, excessive pooling of oral secretions, or by placing a few drops of colored food dye on the tongue and observing for aspiration or penetration. Laryngeal sensation and protective reflexes can be further assessed by the addition of sensory testing (FEES-ST) in which graded bursts of air are applied to an aryepiglottic fold while observing for a laryngeal adductor response. This allows FEES to evaluate children who may aspirate oral secretions or to assess a nonorally feeding child’s safety to begin eating by mouth. Detection of aspiration through a laryngeal cleft can be improved by FEES due to its superior visualization of laryngeal anatomy. FEES is particularly useful in the assessment of postoperative aspiration risk for a child with a high-grade subglottic stenosis in whom airway reconstructive surgery is being planned. Both radiographic swallow studies and FEES are useful and complementary because of the different types of information they provide.
| Videofluoroscopic Swallow Study | Fiberoptic Endoscopic Evaluation of Swallowing |
|---|---|
| Improves clinical examination of swallowing | Improves the clinical examination of swallowing |
| Evaluates oral, pharyngeal, AND esophageal phases of deglutition | Blind to actual moment of swallow Does not evaluate esophageal phase |
| Limited evaluation of anatomy | Evaluates functional anatomy of swallow |
| Evaluates multiple consistencies | Evaluates multiple consistencies |
| May lack sensitivity: Less eaten → less sensitive | Evaluates airway protective ability and sensation (even if the patient does not eat) |
| Feeding recommendations made at time of study | Feeding recommendations made at the time of study |
| Widely available | Not widely available |
| Radiation exposure | No radiation |
| Not portable, noninvasive | Portable but invasive |
| Good caregiver feedback |
Aspiration of Gastroesophageal Reflux
Not all aspiration occurs directly via dysfunctional swallowing. There is a well-documented relationship between GER and chronic respiratory symptoms, such as wheezing, chronic cough, nocturnal cough, apnea, and recurrent chest infections. While there are multiple possible mechanisms for GER-related respiratory symptoms, it is clear that chronic aspiration of gastric contents does occur. The effect of chronic microaspiration of acidic material on the development of chronic lung injury is not entirely clear. With reflux aspiration, there are other factors besides pH; pepsin, bile acids, and food particulates are all present in gastric fluid and may play a role in the pathophysiology of lung injury. Experimental instillation of weakly acidic liquid (pH > 2.5) into the lungs of animals results in an immediate inflammatory response and pneumonitis. The acute effects of a single small-volume instillation subsequently resolve. In an animal model of chronic aspiration, histopathologic changes were completely independent of acidity and were more related to the presence of the food particulates. If it is the gastric contents themselves, independent of acidity that results in lung injury, then acid suppression may not prevent the chronic lung injury from aspiration. In addition, the use of acid-suppressing medications increases gastric colonization by bacteria and may result in aspiration of material with greater bacterial density. This potential has been demonstrated in multiple adult studies of ventilator-associated pneumonia, but not in the single prospective trial in a pediatric intensive care unit.
GER is quite common in children with chronic respiratory diseases. The risk of aspiration from reflux is increased when there is coexisting swallowing dysfunction, decreased laryngeal sensation, tachypnea, or upper airway obstruction. GER and aspiration may also occur in cases of esophageal dysmotility, compression, or stenosis, and these cases are particularly difficult to manage.
Evaluation of Reflux Aspiration
There are several diagnostic modalities available for the diagnosis of GER, yet none are sufficiently sensitive and specific to reliably prove aspiration. While a certain amount of acid exposure may be expected to cause esophagitis, the establishment of norms for reflux aspiration is not possible. Certainly, some individuals may have a moderate amount of reflux and not aspirate, while others may protect their airways so poorly that any amount of reflux results in aspiration and lung injury. Therefore episodes of reflux to or above the upper esophageal sphincter should be thought of as opportunities to aspirate, rather than proof of aspiration itself.
Biomarkers of Aspiration
Biomarkers obtained from the lungs have been sought and evaluated in order to identify children with significant aspiration, especially those who are suspected of aspirating refluxate. The most extensively studied biomarker is the calculation of a quantitative index of lipid-containing macrophages in BAL fluid. Theoretically, an increased prevalence of lipid-filled macrophages in the lower airway suggests aspiration of food during swallowing or following reflux from the stomach. While several studies have found higher levels of lipid in the BAL of children with chronic aspiration than those without, many others have not. This inconsistency is even more striking viewed across studies, even when the methodology for lipid-laden macrophage index (LLMI) is the same ( Fig. 76.3 ). This variability may represent an inherent limitation in the LLMI itself, it may reflect differences in groups characterized as aspirators due to lack of a gold standard, or it may demonstrate that the presence of GER and respiratory symptoms only presumes aspiration as the mechanism. This last point is highlighted by two studies evaluating the correlation of proximal reflux events, detected by esophageal impedance and pH monitoring, to LLMI. Borrelli and colleagues found correlation between reflux episodes to the proximal esophagus (total and nonacid) in children with recurrent consolidation, asthma, and laryngotracheitis, though only two subjects had LLMI greater than the commonly cited threshold of 100. Rosen and coworkers also evaluated children with possible GER and respiratory symptoms. The authors compared proximal reflux events between those that had LLMI greater than and less than 100 and found a trend toward fewer events in those with LLMI greater than 100. We conclude that the overall sensitivity and specificity for LLMI to diagnose aspiration is poor.
