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Chronic Aspiration Without Gastroesophageal Reflux as a Cause of Chronic Respiratory Symptoms in Neurologically Normal Infants^*

^* From the Division of Pulmonary Medicine (Drs. Sheikh, Allen, Shell, Iram, Castile, and McCoy), Department of Pediatrics, Ohio State University College of Medicine, Columbus, OH; and the Department of Speech Pathology and Audiology (Ms. Hruschak), Children’s Hospital, Columbus, OH.

Correspondence to: Shahid Sheikh, MD, Assistant Professor of Pediatrics, Ohio State University, Division of Pulmonary Medicine, Department of Pediatrics, Children’s Hospital, ED 434, 700 Children’s Dr, Columbus, OH 43205; e-mail: SheikhS{at}Pediatrics.ohio-state.edu

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Objective: To describe 13 neurologically normal infants with chronic respiratory symptoms who had swallowing dysfunction with silent chronic aspiration without gastroesophageal reflux (GER) as the cause of their respiratory symptoms.

Background: Infants with neurologic disorders and infants with GER are known to have chronic respiratory symptoms. Isolated swallowing dysfunction and aspiration without GER in neurologically normal infants have not been widely reported.

Design: Retrospective chart review.

Setting: A tertiary pulmonary-care center at a children’s hospital.

Patients: One hundred twelve otherwise healthy infants referred for respiratory symptoms who underwent esophageal pH studies and videofluoroscopic swallow studies (VSSs).

Methods: The records of infants referred between January 1997 and December 1999 to the Department of Pediatric Pulmonology who underwent 24-h esophageal pH monitoring and VSS as part of an evaluation for recurrent stridor and/or wheezing were reviewed. Significant GER was diagnosed if the percentage of time with esophageal pH < 4 was > 6%. Infants included in the study presented with recurrent respiratory symptoms, were born at term, were neurologically normal, had normal results of esophageal pH studies, but had abnormal results of VSSs (n = 13).

Results: All 13 infants presented with a variety of recurrent respiratory symptoms including wheezing and intermittent stridor. Ten of 13 infants had spitting and/or choking episodes with feeding. The mean (± SD) age at the onset of symptoms was 2.0 ± 1.6 months, and the mean age at VSS was 5.9 ± 3.4 months. All 13 infants had normal results of 24-h esophageal pH studies but had abnormal results for VSSs. All infants had evidence of swallowing dysfunction and direct silent aspiration of liquids with thin consistency. Six infants also were aspirating liquids with thick and/or semi-thick consistencies. None of the infants had evidence of structural anomalies on esophagograms. Nine infants were treated with thickened food, and in four infants oral feedings were stopped. Three of these infants required nasojejunal feeding, and one infant required gastrostomy tube feeding. VSSs were repeated every 3 months. In all infants, swallowing dysfunction resolved within 3 to 9 months. All infants tolerated the resumption of oral feeding. Videofluoroscopic documentation of the resolution of aspiration was followed by the resolution of respiratory symptoms in all infants.

Conclusion: There is a subgroup of otherwise healthy infants, presenting with wheeze and/or stridor, who have isolated swallowing dysfunction and silent aspiration as the cause of their respiratory symptoms.

Key Words: aspiration • gastroesophageal reflux • stridor • swallowing dysfunction • wheezing

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Aspiration can be a problem in newborn infants, especially those born prematurely with the inability to coordinate their suck, swallow, and breathing.¹ By 34 weeks of gestational age, however, most infants are able to perform these functions to begin bottle-feeding or breast-feeding.² The maturation of oral and pharyngeal anatomy and the evolution of the suckling process develop parallel to the development of the brain and nervous system.³ When this process falters, these children may develop gagging, regurgitating, or choking during feeding and may fail to thrive. They may also present with recurrent respiratory infections and wheezing.^{4 5 6} Neurologically impaired children are at high risk for aspiration because of a lack of maturation of neuromuscular coordination of the oral and pharyngeal muscles,^{7 8} which is complicated by the increased prevalence of gastroesophageal reflux (GER) in this group.^{9 10} Neurologically normal children with GER are also at an increased risk of aspiration and may present with significant respiratory symptoms.¹¹ The prevalence of reflux as a cause for respiratory disease continues to be investigated.^{6 11 12 13 14}

In our study, we describe a subgroup of neurologically normal infants who were born at term without GER and who aspirate enough to cause chronic wheezing and stridor. These infants had silent aspiration due to isolated swallowing dysfunction. The diagnosis required an intensive evaluation of the swallow function using videofluoroscopic techniques, but with proper treatment these infants were quickly free of symptoms.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
The records of otherwise healthy infants who were referred between January 1997 and December 1999 to the Department of Pediatric Pulmonology at Children’s Hospital in Columbus, OH, who underwent 24-h esophageal pH monitoring and videofluoroscopic swallow studies (VSSs) as part of an evaluation for recurrent stridor and/or wheezing were reviewed (n = 112) with the approval of the Children’s Hospital Institutional Review Board. The Children’s Hospital Pulmonary Division sees approximately 5,000 children each year, of whom 550 to 600 are new patients. Approximately 100 children (75 to 80% of them infants and young toddlers) are referred for VSS and/or prolonged pH monitoring every year. Approximately 40% of the children referred for these studies had an underlying diagnosis of asthma, 5 to 8% had recurrent stridor, and others were observed for prematurity with, for instance, bronchopulmonary dysplasia, cystic fibrosis, or recurrent pneumonia. During the nearly 2-year period of this study, 228 infants underwent prolonged esophageal pH monitoring and 196 infants underwent VSS. Of the 183 infants who underwent both procedures, 112 were otherwise healthy, full-term infants who had been referred for wheezing, chronic cough, and/or stridor. The charts of these 112 infants were reviewed for this study. Significant GER was diagnosed if the time with esophageal pH < 4 was > 6%.^{15 16} Infants included in this study (n = 13) were healthy except for recurrent stridor and/or wheezing, nonresponse to the usual therapies, and normal results of the esophageal pH study but abnormal results of the VSS. Infants with VSS demonstrating direct aspiration were included in the study. Infants with VSS suggestive only of laryngeal penetration or other minor abnormalities were not included in the study. Exclusion criteria included the following: prematurity (ie, < 36 weeks of gestational age); previous mechanical ventilation; cerebral palsy; developmental delay; known neuromuscular impairment; obstructive sleep apnea; previous surgery; congenital malformation; or chromosomal abnormality. Demographic data and the results of esophageal pH studies and VSSs were obtained from patient records. All infants were evaluated prospectively by developmental pediatrics and pediatric neurology investigators.

The VSS
At our institution, approximately 900 VSSs are performed each year on 350 to 400 children, of whom 60 to 70% are infants and toddlers. Approximately 35% of the children studied have significant neurologic deficits, 35 to 45% have a history of severe prematurity, and 20 to 25% are otherwise healthy patients referred for wheezing with or without GER. Approximately 60 to 65% of the patients with neurologic deficits have abnormal VSS results, almost 50% of patients with underlying severe prematurity have abnormal study results, and 30 to 35% of otherwise healthy patients with respiratory symptoms with or without GER have abnormal study results.

VSSs were performed to assess the oral, pharyngeal, and esophageal phases of swallowing and to rule out or further analyze swallow dysfunction. A multidisciplinary approach included a diagnostic team of an occupational therapist, speech pathologist, and a radiologist. Included in the assessment was a history of feeding and swallowing issues along with an indication of present status, an evaluation of structural, sensory, and motor function related to feeding and swallowing, a report or direct observation of the current feeding status, and the results of the VSS.

A complete history was obtained to identify issues related to feeding and swallowing, and written informed consent was obtained from the parent or legal guardian in preparation for the actual VSS. The guardian was asked to bring age-appropriate and familiar feeding utensils as well as some preferred foods and any foods that were known to cause difficulty. The speech pathologist involved in the assessment prepared the foods by mixing the required amount of barium and insuring that a variety of consistencies was available for the test. Thin liquid barium was 70% concentrated (Barosperse barium sulfate suspension; Lafayette Pharmaceuticals; Lafayette, IN). This concentration was considered to be semi-thick by adding a half-tablespoon of infant rice cereal per ounce of thin liquid barium. A thick consistency of liquid was achieved by adding one tablespoon of infant rice cereal per ounce of thin liquid barium. Positioning in a seating system that most closely simulated their normal feeding position was achieved with the guidance of the occupational therapist. Comparisons were made of both the habitual and optimal position for feeding.¹⁷ Once all these components were in place, the radiologist began the fluoroscopic procedure.

The occupational therapist or parent/guardian fed the infants during the study. The procedure was documented on videotape for visual interpretation. Throughout the assessment, the occupational therapist recorded observations regarding the oral phase, assessing the ability to extract from the nipple, bolus propulsion, and whether external support was needed. The speech pathologist and radiologist interpreted the pharyngeal and esophageal phases, assessing propulsion, timing of swallow initiation, presence or absence of laryngeal penetration, peristaltic movement, and efficiency of velar closure. Differentiation of direct vs indirect aspiration was noted along with swallow delay, pooling, residue, possibility of cricopharyngeal dysfunction, and reverse motility, and there was consideration of whether compensatory techniques such as chin tuck were needed. In addition, the radiologist documented structural issues that may be related to swallow malfunction. To ensure continuity, the speech pathologist documented a written record of positioning, each consistency presented, how presented, and observations regarding the transit in the pharyngeal and esophageal phase.

The swallow was judged to be insufficient and requiring alterations in texture or presentation if episodes of deep laryngeal penetration below the vocal cords exceeded 25% of presentations, if pooling and delayed initiation exceeded 25% of presentations, or if direct or indirect aspiration was observed. If significant changes were required (such as changing from thin to thick liquids), written instructions were provided to the child’s caregivers to ensure consistency in the food preparation. Artificial food thickeners and resources for obtaining them were provided as well.

We used the following standards of liquid consistency. Thin consistency was regular formula. Semi-thick consistency was obtained by adding one-half tablespoon of infant rice cereal per one ounce of regular formula. Thick consistency was obtained by adding one tablespoon of infant rice cereal per one ounce of regular formula, and extra-thick consistency was obtained by adding one tablespoon plus one teaspoon of infant rice cereal per ounce of regular formula. The continuation of oral feeding required that the patient be able to take enough liquids to meet their hydration needs. If oral feeding could not be maintained, a nonoral route was chosen, and non-nutritive oral stimulation with a pacifier, Nuk massage brush (Gerber Products; Fremont, MI), or Infa-Dent (Lactede; Rancho Dominguez, CA) was taught to the parents. Children who required nonoral feeding were generally seen for a reassessment in 4 to 8 weeks to re-establish oral feedings as soon as possible.

Diagnostic Evaluation of GER
All infants were evaluated for acid GER by prolonged esophageal pH monitoring using criteria described by Sondheimer¹⁵ using a pH probe electrode placed 3 to 4 cm above the gastroesophageal junction. The position of the probe was verified by a chest roentgenogram. The activity, feeding, and asthma medications were continued as usual during the tests. Significant acid reflux was defined as a reflux index (ie, the percentage of time esophageal pH was < 4) of > 6% (normal reflux index, 3.4%; 95th percentile), or more than five reflux episodes of > 5 min duration, or any reflux episode of > 30 min duration.^{15 16}

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Of 112 infants in this study, 26 infants (23%) had abnormal results for both the 24-h esophageal pH monitoring study and the VSS, 55 infants (49%) had normal results for both the 24-h esophageal pH monitoring study and the VSS, 18 infants (16%) had abnormal results for the 24-h esophageal pH monitoring study but normal results for the VSS, and 13 infants (11.6%) had normal results for the 24-h esophageal pH monitoring study but abnormal results for the VSS. We focused on the last group, and the characteristics and symptoms of patients in that group are described in Tables 1 and 2 . The mean (± SD) age at which the esophageal pH study and VSS were performed was 5.9 ± 3.4 months. The mean weight was 7.5 ± 2.4 kg, and the mean height was 66.5 ± 5.9 cm. The mean percentiles for weight, height, and weight/height ratio for both boys and girls were between the 25th and 50th percentiles. The nature of the swallowing dysfunction observed is described in Table 3 .

Patient management is described in Table 4 . Nine of 13 infants were treated with thickened food. In the remaining four infants, oral feedings were stopped. Three of these infants received nasojejunal (NJ) feedings, and one infant required a gastrostomy tube. VSSs were repeated every 3 months. In all infants, swallowing dysfunction resolved within 9 months of the diagnosis. All infants tolerated the resumption of oral feedings. At their 3-month follow-up VSS study, all but 1 of the 13 infants demonstrated improvement in their swallowing function. All infants who initially demonstrated aspiration with only thin consistencies had resolution of swallowing dysfunction and aspiration and were able to resume regular feedings by their 3-month follow-up examination. At the 6-month follow-up studies, all infants who aspirated while receiving semi-thick and thick consistencies of food had marked improvement of swallowing dysfunction and aspiration, and two of three NJ tube feedings were replaced with oral feeding. By the 9-month follow-up studies, aspiration and swallowing dysfunction had finally resolved in all infants. Even those patients who had required ing with a gastrostomy tube or NJ tube then could be fed successfully with regular oral diets.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
In a retrospective review⁸ of patients undergoing a videofluoroscopic-modified barium swallow study at Children’s Hospital of Buffalo, NY, it was noted that the vast majority of patients who aspirated were dependent on caregivers for feeding (90%) and had a diagnosis of cerebral palsy (71%). Importantly, it was noted also that many of these aspirators did so silently (ie, aspiration was not accompanied by cough or choking). Abnormalities in pharyngeal swallow function, such as reduced peristalsis and pooling of material in the vallecula, were commonly seen in the aspirating patients.⁸

Aspiration may present with gagging, choking, or coughing during feedings, apnea and bradycardia (particularly in the young infant), wheezing or chronic noisy breathing, recurrent episodes of pneumonia or bronchitis, chronic lung disease, excessive salivation, or failure to thrive.^{1 2 3 4 5 6 7 8} The possibility of aspiration, secondary either to GER or due to primary direct aspiration during swallowing, should be consideration in the differential diagnosis of many young children presenting with chronic respiratory symptoms. In our initial cohort of 112 neurologically normal, term infants presenting to a pediatric pulmonary subspecialty group for an assessment of chronic wheeze, chronic cough, and/or stridor, 23% had both abnormal results of 24-h esophageal pH monitoring and aspiration on a VSS, 16% demonstrated GER without aspiration, and 11.6% had aspiration during swallowing without coexistent GER. It is likely that different mechanisms may have resulted in the respiratory symptoms seen in each of these groups, and, depending on the type of abnormality, the direct aspiration of foodstuffs, the aspiration of acid reflux material, and/or the stimulation of vagally mediated irritant receptors in the lower esophagus alone or in combination may have been involved.

Our data also demonstrate that in healthy infants with silent aspiration without GER, chronic respiratory symptoms resolved once swallowing dysfunction and silent aspiration were identified and treated. It is well-recognized that apparently neurologically normal children can have significant respiratory impairment due to GER-related aspiration.¹⁸ It is generally presumed that isolated swallow dysfunction is seen primarily in children with some type of local anatomic abnormalities (congenital, or acquired due to local trauma or infection) or with some form of CNS dysfunction.^{7 8} Swallowing incompetency, therefore, is suspected primarily in those children with additional neurologic risk factors, such as prematurity, CNS injury, hydrocephalus, developmental delay, or cerebral palsy.^{4 5 7 8} In this study, we have demonstrated that otherwise healthy children also can be aspirators. The prevalence of swallow dysfunction and silent aspiration in this healthy population is not well-established, because this population of children is generally not considered at risk for dysphagia and testing is not performed. Less recognized is the potential for apparently neurologically normal children to experience transient difficulty with swallowing as an isolated cause of their respiratory complaints. We have identified a group of 13 infants, neurologically normal with normal growth and development, who presented with respiratory symptoms and appeared to have an isolated abnormality of their swallow function. These infants, on average, became overtly symptomatic by 2 months of age with wheeze, cough, stridor, recurrent pneumonia, and/or apnea. Approximately half of them (6 of 13 infants) had symptoms suggestive of frank aspiration, such as gagging and spitting, or choking during feedings. Of the 13 infants, 4 experienced feeding-related vomiting and 3 had no recognized feeding problems at all. The persistence of symptoms led eventually to VSS by an average of 5.9 months of age, demonstrating the aspiration of thin liquids in all infants and of liquids of thicker consistency in six infants. Our group responded well to the alteration of their feeding method. Thirteen infants could be managed on thickened feedings alone, and 4 required a temporary period (6 to 9 months) of NJ or gastrostomy tube feedings due to their inability to safely handle any consistency of liquid. With these feeding alterations, all patients experienced an improvement in or resolution of their respiratory complaints. Within 3 months, 9 of the 12 patients originally receiving asthma medications at the time of diagnosis had been successfully weaned from this therapy. In addition, within 3 months, all but one of the 13 infants had demonstrated improvement in their swallowing function, and all with aspiration on liquids of thin consistency were advanced to regular diets.

The cause of swallowing dysfunction in these infants is unclear. These infants were not premature (mean gestation age, 38.5 ± 1.2 weeks), there was no evidence of global neurologic dysfunction (none had cerebral palsy or developmental delay), there was no history suggestive of an incident that may have traumatized the pharyngeal area (none had undergone surgery or received mechanical ventilation), and there was no evidence of GER (all had normal results of esophageal pH monitoring). These infants appear to have had a form of delayed neuromuscular incoordination that either improved on its own or because of an alteration in feeding patterns and the minimization of the ongoing insult.

Our experience emphasizes the need to evaluate infants presenting at an early age with chronic respiratory symptoms, particularly unexplained wheezing, for swallowing dysfunction. Significant swallowing dysfunction can occur in some infants in the absence of abnormal GER, neurologic findings, developmental delays, or overt feeding difficulties. It is most clearly identified by the use of VSS and will typically improve with time. Treatment involves altering the feeding method to thickened feedings or, sometimes, using NJ or gastrostomy tube feeding. Further work is needed to identify the underlying cause of this infantile swallowing dysfunction and to identify under what circumstances more aggressive therapies or neurologic evaluations may be indicated should spontaneous improvement in function fail to occur.

	Footnotes

 
Abbreviations: GER = gastroesophageal reflux; NJ = nasojejunal; VSS = videofluoroscopic swallow study

Received for publication October 4, 2000. Accepted for publication May 8, 2001.

	References

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