Silent aspiration prominent in children with dysphagia

INTERNATIONAL JOIWJALOF

Pediatric

ELSEVIER SCIFNCL IRELAND

International

Journal of Pediatric Otorhinolaryngology 28 (1994) 173-181

Silent aspiration prominent in children with dysphagia Joan Arvedson* a3c7d, Brian Rogers b*e,Germaine Bucke, Paulette Smart e, Michael Msall b3e “Speech-Language-Hearing

and Pediatrics Department, hRobert Warner Rehabilitation Cenirr,

Children’s Hospilal of Buffalo, 219 Bryant Street, Buffalo 14222, NY, USA ‘Department of Otolatyngology, School of Medicine and Biomedical Sciences, ‘Deparlmeni of Communicative Disorders and Sciences, School of Social Sciences. School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, NY, USA eSchool of Medicine and Biomedical Sciences, State University of New York at B@zlo, Bvflalo, NY, USA (Received

24 February

1993; accepted

17 May 1993)

Abstract

Children with neurologically-based dysphagia are at high risk for silent aspiration. Aspiration can lead to complications such as acute pneumonia and chronic lung disease. Thorough evaluation of the oral, pharyngeal, and esophageal phases of swallowing is crucial for patients with dysphagia. The videofluoroscopic modified barium swallow study (MBS) is the procedure of choice for children to delineate the pharyngeal and upper esophageal phases of the swallow that can only be inferred by bedside clinical assessment. This study describes attributes of aspiration and pharyngeal motility in a large sample of infants and children assessed with MBS. Aspiration was observed in 48 (26%) of 186 children, primarily on liquid before or during swallows. Aspiration was trace (less than 10% of a bolus) and silent in 94%. Relationships to clinical history and implications for management are discussed. Given the lack of objective clinical information to identify children at risk for aspiration, MBS should be considered in all children with severe dysphagia to rule out or confirm aspiration. Key words: Aspiration; Swallowing dysfunction; Infants and children; Dysphagia; Deglutition; Pediatrics, developmental; Radiography; Videofluoroscopy; Clinical evaluation

* Corresponding author, at the following address: Department ren’s Hospital, 219 Bryant Street, Buffalo, NY 14222, USA.

01655876/94/$07.00 0 1994 Elsevier Science Ireland SSDI 0165-5876(93)00962-E

of Speech-Language-Hearing,

Ltd. All rights reserved.

The Child-

174

J. Arm&on et al. /Int. J. Pediatr. Otorhinolaryngol. 28 (1994) 173-181

1. Introduction Dysphagia, or dysfunctional swallowing, is common in children with severe cerebral palsy and multiple disabilities [ 181. It can also occur in at-risk neonates and children with a variety of neurological deficits, and in some instances, with structurally-based problems. Dysphagia may be characterized by dysfunction in oral, pharyngeal, and esophageal phases of the swallow. During oral feedings, children with dysphagia are at risk of aspiration, defined as the entry of material into the airway below the level of the true vocal folds. Aspiration may also arise from gastroesophageal reflux [ 161. Respiratory distress has been observed during oral feeds in children with multiple disabilities and dysphagia [5,11]. Hypoxemia has been demonstrated in adults with severe neurological disabilities [ 191and in children with severe cerebral palsy during oral feeding [ 171. Complications of aspiration can include acute pneumonia and chronic lung disease [5,11]. Evaluation of the oral, pharyngeal, and esophageal phases of swallowing is essential for patients with dysphagia. The bedside or clinical assessment reviews the patient’s history, medical status, developmental skills, and oral-motor function. It may include swallows of food or liquid, depending on the perceived risk for possible aspiration that may be undetected at the bedside [9]. Characteristics of pharyngeal motility and airway protection during oral feedings have not been reliably assessed by bedside evaluation [7]. The videofluoroscopic modified barium swallow (MBS) study is the procedure of choice in evaluation of the pharyngeal and esophageal phases of deglutition [2,6,8-10,211. The MBS can characterize the duration of oral and pharyngeal transit times, pharyngeal motility, presence or absence of material pooled in the vallecula and/or pyriform sinuses prior to a swallow or as residue in the pharyngeal recesses after a swallow, and presence or absence of aspiration. The occurrence of aspiration on specific food textures, and whether these occurrences of aspiration are noted before, during, or after swallows, all have implications for management. Reports of radiographic studies of deglutition in children with dysphagia have been limited [1,3,4,20]. These studies reported on a small number of children with multiple disabilities. Pharyngeal phase abnormalities were often influenced by the texture of food swallowed. These studies emphasize the need for standardized evaluations of the oral and pharyngeal phases of deglutition with specific food textures. Videofluoroscopy aids in delineation of aspiration, although the underlying neurological mechanisms of aspiration in children with dysphagia are not yet well understood. It is known that afferent sensory fibers to the brain stem swallowing centers provide taste and sensory information from the tongue and oral-pharyngeal mucosa, as well as proprioceptive information from the musculature involved [13,14]. Aspiration has been shown to be influenced by the texture of substances swallowed [3,4]. Additionally, specific deglutition abnormalities and the relationship of the abnormalities to texture of substances may be markers of strength and coordination of the swallowing mechanism.

J. Arvedson et al. /Int. J. Pediatr. Otorhinolaryngol.

28 (1994)

173-181

115

2. Purpose The purpose of this study was to characterize the clinical and radiographic characteristics of aspiration in children with dysphagia. Feeding histories, health status, and neurodevelopmental profiles of a large cohort of children with dysphagia and aspiration were reviewed. The overall goal was to examine the relationships among aspiration, deglutition abnormalities, and specific food textures. 3. Method A retrospective review of 186 consecutive children who were evaluated with videofluoroscopic modified barium swallow studies at the Children’s Hospital of Buffalo from 1989 to 1991 was completed. Only initial studies were considered for this report. Patients were referred by physicians in community and tertiary care facilities. The mean age was 5.8 years with a standard deviation of 5.9 years. Ages ranged from 2 days to 21 years. The group consisted of 59% males. The most common reasons for referral (Table 1) were coughing, choking, or trouble breathing during oral feeds (48O), and/or concern for aspiration (46%). Slow oral feeds, gagging during feeds, and food refusal were present in 14-25%. Most of the children had significant dysphagia and developmental disabilities. The cohort included 132 (71%) who received total oral feeds and 54 (29%) who received tube feedings with or without some limited amount of oral feeding. Most children (87%) required assistance at mealtime or were totally dependent on others to feed them. A high percentage of children had diagnoses of cerebral palsy (48%) and mental retardation (54%). These diagnoses of cerebral palsy and mental retardation were confirmed by a developmental pediatrician. A total of 89% had recognized developmental disabilities or delays. The fluoroscopic procedure was carried out by a speech-language pathologist (SLP) and a radiologist according to the protocol of Logemann [lO,l l] with minor modifications for children. A Philips Super 80 CP generator and conventional fluoroscopy unit were used with digital spot imaging and laser cameras. The dynamic image was recorded on a 3/4-inch VHS videotape. Lateral views were used in

Table I Reasons for referral Reason

for videofluoroscopic

modified

for referral”

Coughing, choking oral feeds

swallow Percent

or trouble

Concern for aspiration Slow oral feeding (>40 Gagging during feeds Food refusal “Not mutually

barium

exclusive.

min)

breathing

during

48 46 25 14 14

studies

(n = 186)

176

J. Arvedson et al. /Ink J. Pediatr. Otorhinolaryngol. 28 (1994) 173-181

all subjects. An anteroposterior (AP) view was used occasionally when asymmetry was suspected in the pharyngeal phase. Each child was positioned to simulate the typical feeding position(s) as well as the optimal feeding position. Children were usually positioned upright in a Tumbleform seat with head support, as needed. Infants were positioned in an semi-upright position (approx. 60-75”) in a small Tumbleform seat. Food textures used in routine oral feedings were studied. Food samples were impregnated with barium for contrast. Barium sulfate liquid was used for liquid swallows. Barium esophatrast was mixed with other textures for spoon feeding. Solids were coated with barium esophatrast. Solids included small pieces of graham cracker, bread, sandwich, or meat. The texture reported to be tolerated best was usually given first, followed by those of greater concern. In children who typically were spoon fed at home, the amount per presentation was approximately onequarter to one-third of a teaspoon via spoon. One to three swallows per texture were observed. Sampling included liquid, pureed, and solid textures in 54%, and liquid and/or pureed textures in 46%. The presence of trace aspiration with a particular texture did not automatically mean that the study was terminated. Some children showed improvement after a few swallows. The study usually proceeded with assessment of other textures to determine if aspiration was texture-specific. Fluoroscopy time was kept to 2 min or less whenever possible. Infants were usually assessed with liquid via nipple. Total fluoroscopy time was usually less than 30 s. The SLP and radiologist both made observations relating to the timing of the swallow, coordination in oral and pharyngeal phases of the swallow, pharyngeal peristalsis, presence or absence of material pooled in the pharyngeal recesses prior to a swallow or residue in the pharyngeal recesses after the swallow, and esophageal transit time [ 11. Transit times for all phases were estimated by both the SLP and the radiologist. On-line timers were not used. Occurrences of aspiration before, during, or after swallows of varied textures were documented. Findings were shown to care givers and professionals who accompanied a child immediately after the procedure. Oral phase observations included estimation of oral transit time and tongue function. The oral phase was considered to be delayed when the duration of posterior propulsion of a bolus from the tongue dorsum to the tonsillar pillars was estimated to be greater than 3 s. Tongue control abnormalities included excessive tongue thrusting and pumping, limited lateral movement with solid food, and lack of efticient sucking via nipple in infants. Piecemeal deglutition described fragmentation of the bolus over the dorsum of the tongue. Multiple swallows were noted when 3 or more swallows were produced per bolus. Pharyngeal phase deficits included delayed swallow production (bolus remaining in the pharynx for 3 s or more prior to a swallow), pooling in the vallecula and/or pyriform sinuses prior to swallows, residue in the vallecula and/or pyriform sinuses after swallows, reduced pharyngeal peristalsis, and aspiration. Pharyngeal peristalsis was deemed to be reduced when the bolus took 2 s or more to move through the pharynx, usually resulting in pharyngeal residue after swallows. It was noted whether aspiration occurred before, during, or after swallows, and with which textures. Aspiration was considered ‘trace’ when less than an estimated 10% of a barium

J. Arvedson et al. /Int. J. Pediatr. Otorhinolaryngol. 28 (1994)

173-181

177

Table 2 Texture-specific aspiration in patients assessed with three textures (n = 38) Texture

Percent

Liquid alone Liquid and pureed All textures Liquid and solid Pureed and/or solid

48 18 I8 8 8

bolus entered the trachea below the level of the true vocal folds. This volume was estimated from lateral two-dimensional images, and was not quantified objectively. Aspiration was considered ‘silent’ when no observable cough occurred within 20 s of an aspiration incident. Data analysis was accomplished by descriptive statistics to include frequencies, cross-tabulations, and measures of central tendency using SPSSPC statistical software package [ 151. Statistical significance (P < 0.05) was calculated by use of Yates corrected x2 statistic, or Fisher’s exact test (two-tailed) for cell sizes less than five. The x2 contingency test was used for determining statistical significance for tables larger that 2 x 2 (R x c). 4. Results Videofluoroscopic modified barium swallow studies revealed aspiration in 48 of 186 children (26%). The associated diagnoses in the children who aspirated (n = 48) include cerebral palsy (71%), other developmental disabilities (lo%), postnatal CNS injury (8%), neuromuscular disease (7%), neuroblastoma (2%). There were no significant differences in the frequency of aspiration in various age groups (< 1 year, l-3 years, and > 3 years). Therefore, the data were collapsed for the age variable. Assistance with oral feeding or total dependence on others for oral feeds was a characteristic in 90% of the children who aspirated. Almost all aspirations were of trace amounts and silent (94%). The aspiration occurred before or during swallows in 58%, and after swallows in 42’/0. Table 3 Timing of aspiration related to texture (n = 48) Timing of aspiration with swallow

Before During After Varying times

Liquid (n = 41)” u/o

(n = 23)”

u/u

Solid (n = 9)” ‘%

I5 44 I9 22

17 I7 48 I8

22 33 II 34

“Number of aspirators per texture

Pureed

178

J. Arvedson et al. /Int. J. Pediatr. Otorhinolaryngol. 28 (1994)

173-181

In the children who were assessed with all three textures (n = 38), aspiration was most prominent for liquid (Table 2), either alone or with some other texture (74%). Aspiration on liquid alone was found in nearly half the group (48%), on liquid and pureed in 18%, and on liquid and solid in 8%. Only 8% aspirated only on pureed and/or solid textures. The other 18% showed aspiration on all three textures. The timing of aspiration (n = 48) of specific food textures was examined (Table 3). Liquids were more commonly aspirated during swallowing (44%). Pureeds were aspirated more often after swallows (48%). Finally, solids were more commonly aspirated during (33%) and before (22%) swallows. The group with aspiration (n = 48) was compared with the larger group of nonaspirators (n = 138) (Table 4). Nearly all children who aspirated had both oral and pharyngeal phase deficits (98%). However, oral and pharyngeal phase deficits were found in 71% of the children who did not aspirate. Various aspects of pharyngeal motility were significantly more common in subjects with aspiration (P < 0.001). Major pharyngeal motility deficits included delay in the production of a swallow in 94% of those who aspirated and 65% of those without aspiration. Nearly all subjects with aspiration had pooling of material into the vallecula (94%) and some showed pooling into the pyriform sinuses prior to a swallow. Residue after swallows was evident in 79% of the children with aspiration and in only 35% of those without aspiration. Multiple swallows to attempt to clear the pharyngeal recesses were made in 79% of the group with aspiration, but in only 50% of the group without aspiration. Reduced pharyngeal peristalsis was found in 67% of those who aspirated but in only 16% of those who did not aspirate. The relationships among aspiration, feeding concerns, and developmental diagnoses were examined (Table 5). Children who aspirated had a significantly higher prevalence of respiratory distress during feeds and severe disabilities (P < 0.05). All but one of the aspirators (96%) were dependent feeders and 71% had a diagnosis of cerebral palsy compared with the group of non-aspirators in which 83% were dependent feeders and 41% had a diagnosis of cerebral palsy. However, the sen-

Table 4 Percent comparison of oral and pharyngeal phase abnormalities by aspiration Aspiration

Abnormality

Oral phase Pharyngeal phase Delayed swallow Pooling before swallows Residue after swallows Multiple swallows per bolus Reduced peristalsis All associations significant at P

c

0.001.

Yes (n = 48)

No (n = 138)

98 98 94 94 79 79 67

71 72 65 71 35 50 I6

J. Arvedson et al. /Int. J. Pediarr. Otorhinolaryngol. 28 (1994) Table 5 Percent comparison History

of history

variables

179

173-181

by aspiration

variable

Aspiration Yes (n = 48)

Cough, choke, or respiratory Concern for aspiration

No = 138)

problems

Dependent feeding Cerebral palsy All associations

significant

at P < 0.05.

sitivity and specificity for these clinical variables were generally low (Table 6). Although the sensitivity was high (98%) for dependent feeding, the specificity was low (15%). Predictive values for these variables were also low, ranging from 33% to 38%. 5. Discussion Aspects of deglutition and aspiration that may have clinical management implications for children with dysphagia are characterized by videofluoroscopic modified barium swallow studies, Aspiration appears to occur commonly in children with severe developmental disabilities and dysphagia. However, feeding histories and clinical observations are not reliable for early identification. Aspiration usually occurs in children with significantly disordered pharyngeal motility. Aspiration is usually silent and of trace amounts. Children very commonly aspirate a specific food texture and not all textures in their diet. Previous investigations of children with dysphagia and aspiration have had limited numbers of children with multiple disabilities [3,4]. In the present investigation with a large group of children demonstrating aspiration, liquids were more commonly aspirated than any other food texture. This finding supports Loughlin’s [l l] statement that aspiration generally occurs with liquid swallows in pediatric patients. This

Table 6 Sensitivity History

and specificity

for clinical

variable

Cough, choke, or breathing Rule out aspiration Dependent feeding Cerebral palsy

difftculties

history

variables Sensitivity o/o

Specificity u/o

62 67

57 61

98 14

15 56

180

J. Arvedson et al. /Int. J. Pediatr. Otorhinolaryngol. 28 (1994) 173-181

finding is in contrast to the findings of Griggs et al. [3] and Helfrich-Miller et al. [4] who reported that barium paste was more commonly aspirated than any other texture. Given the highly selected population in the present report, the results must be interpreted cautiously. The population consisted primarily of children with multiple disabilities and severe dysphagia. The correlation of findings on modified barium swallow studies to routine daily feedings in children with severe dysphagia remains unclear. Some children are reported to have more difficulty with oral feedings toward the end of meals or later in the day. Future investigations may need to consider the association of fatigue with various measures of pharyngeal motility or aspiration as observed during modified barium swallow studies. Aspiration does not appear to be an isolated event. Aspiration appears to be highly associated with disorders of pharyngeal motility. Both afferent and efferent controls of deglutition may account for food texture-specific aspiration. The pervasive finding of silent aspiration on modified barium swallow studies in children with dysphagia and multiple handicaps has significant implications for management. Silent aspiration can be overlooked if observors expect that the presence of aspiration will include coughing, choking, or respiratory distress during oral feeds. Information from modified barium swallow studies can be helpful in determining potential therapeutic management strategies. Possible strategies to enhance the safety of oral feedings may include changes in rate of feeding and in food textures. Some children may not be safe for total oral feedings, and non-oral feedings become the means for optimizing nutritional status. Recommendations have included oral-motor stimulation to prevent the development of oral hypersensitivity and to include a variety of tastes and textures for sensory stimulation [3]. Stimulation may also facilitate oral-motor function for handling of secretions and dental hygiene. The clinical implications of chronic silent, trace aspiration in children with dysphagia need to be investigated. Considerations of the intricate coordination necessary for efficient swallowing and respiration may lead to the development of physiologically approprite markers of deglutition disorders. Effective strategies are needed in order for caregivers to support their children with dysphagia in maximizing nutrition, psychosocial, and habilitation potential.

6. Acknowledgments The authors thank the physicians and technicians in the Radiology Department of the Children’s Hospital of Buffalo for their cooperation in carrying out the modified barium swallow studies. This study was partially sponsored by The Children’s Guild and the Office of Mental Retardation and Developmental Disabilities of the State of New York. Portions of this study were presented at the meeting of the American Academy for Cerebral Palsy and Developmental Medicine, San Diego, CA, October 1992, and at the Society of Ear, Nose, and Throat Advances in Children, Toronto, Canada, December 1992.

J. Arvedson et al. / Int. J. Pediatr. Otorhinolaryngol. 28 (1994)

173-181

181

7. References Arvedson, J. and Christensen, S. (1993) Instrumental assessment. In: Arvedson J.C. and Brodsky L. (Eds.), Pediatric Swallowing and Feeding: Assessment and Management. Singular Publishing 2 3 4 5 6 I 8 9 10

Group, San Diego, pp. 293-326. Dodds, W.J., Logemann J.A. and Stewart, E.T. (1990) Radiologic assessment of abnormal oral and pharyngeal phases of swallowing. Am. J. Roentgenol. 154, 965-974. Griggs, C.A., Jones, P.M. and Lee R.E. (1989) Videofluoroscopic investigation of feeding disorders of children with multiple handicap. Dev. Med. Child Neural. 31, 303-308. Helfrich-Miller, K.R. Rector, K.L. and Straka, J.A. (1986) Dysphagia: its treatment in the profoundly retarded patient with cerebral palsy. Arch. Phys. Med. Rehabil. 67, 520-525. Jones, P.M. (1989) Feeding disorders in children with multiple handicaps. Dev. Med. Child Neurol. (Annotation) 3 I, 404-406 Kramer, S.S. (1985) Special swallowing problems in children. Gastrointest. Radiol. 10, 241-250. Langmore, S.E. and Logemann, J.A. (1991) After the clinical bedside swallowing examination: What next? Am. J. Speech Lang. Pathol. l(l) 13-20. Linden, P. and Siebens, A.A. (1983) Dysphagia: predicting laryngeal penetration. Arch. Phys. Med. Rehabil. 64, 281-284. Logemann, J.A. (1983) Evaluation and Treatment of Swallowing Disorders. PRO-ED, Austin, TX. Logemann, J.A. (1986) Manual for the Videotluorographic Study of Swallowing. College Hill Press,

12

San Diego. Loughlin, G.M. (1989) Respiratory consequences of dysfunctional swallowing and aspiration, Dysphagia 3, 126- 130. McBride, M.E. and Danner, S.C. (1987) Sucking disorders in neurologically impaired infants: asses-

13 14 15

sment and facilitation of breastfeeding. Clin. Perinatol. 14, 109-130. Miller, A.J. (1982) Deglutition. Physiol. Rev. 62 129-184. Miller, A.J. (1986) Neurophysiological basis of swallowing. Dysphagia Norusis, M.J. (1990) SPSS/PC+ 4.0 Base Manual. SPSS, Chicago.

II

16 17 18 19 20 21

1, 91-100.

Orenstein, S.R. and Orenstein, D.M. (1988) Gastroesophageal rellux and respiratory disease in children. J. Pediatr. 112, 847-858. Rogers, B.T., Arvedson, J., Msall, M. and Demerath, R.R. (1993) Hypoxemia during oral feeding of children with severe cerebral palsy. Dev. Med. Child Neurol. 35, 3-10. Rogers, B., Arvedson, J., Buck, G., Smart, P. and Msall, M. Characteristics of dysphagia in children with cerebral palsy. Dsyphagia (in press). Rogers, B., Msall, M. and Shucard, D. (1993) Hypoxemia during oral feedings in adults with dysphagia and severe neurological disabilities. Dysphagia, 8, 43-48. Sloan, R.F. (1977) The cinefluorographic Dent. Univ. 11, 58-73. Tuchman, D.N. (1989) Cough, choke, swallowing. Dysphagia 3, 11 l-1 16.

study sputter:

of cerebral

palsy deglutition

the evaluation

of the child

patterns.

J. Osaka

with dysfunctional