Swallowing dysfunction (dysphagia) is common in the paediatric population within a wide range of disorders and hinders the provision of adequate nutrition, affecting growth and development leading to significant parental anxiety and family disruption (1–3). Pulmonary aspiration because of swallowing dysfunction (deglutitive aspiration) is the major reason for feeding strategy modification (eg, oral to tube feeding, avoidance of liquids) that can significantly affect quality of life. Furthermore, aspiration can lead to recurrent pneumonia, progressive lung disease, respiratory disability, and potentially death (4). Deglutitive aspiration most often occurs in children with neurological disease, but can also be a cause of recurrent pneumonia, recurrent wheezing, chronic cough, or stridor in neurologically normal infants and children (5).
Safe and effective swallowing is a complex process. After oral acceptance, bolus delivery to the pharynx initiates the pharyngeal swallow reflex and the tongue base propels the bolus backwards, the soft palate closes the nasopharynx, the larynx elevates, vocal folds close, and upper oesophageal sphincter (UES) relaxes and opens to allow the bolus to pass. The pharyngeal contraction then clears bolus residue from the pharynx. Although disrupted effectiveness, duration and/or timing of any of these components can result in aspiration, there is no objective test that can assess swallowing risk without fluoroscopy (4).
Fluoroscopy is the present criterion standard tool for evaluation of direct aspiration in children. The limitations of fluoroscopy relate to exposure to radiation, limited quantifiable indicators, poor predictability of progression to aspiration pneumonia (6,7), and the fact that a normal fluoroscopy cannot entirely guarantee the absence of feed aspiration because of limits on investigation time (4). Moreover, fluoroscopy-based findings such as pharyngeal residue have been described as relatively poor markers of aspiration (8). Observed clinical signs and symptoms (eg, wet voice, wet breathing, cough) have a 33% to 67% sensitivity to predict aspiration of liquids on fluoroscopy (9,10).
The aim of the present study was to evaluate a new approach, pharyngeal automated impedance manometry (AIM), for the objective assessment of pharyngeal and UES function relevant to aspiration in infants and children. AIM uses high-resolution intraluminal manometry combined with impedance measurement and derives pharyngeal pressure–flow variables. These pressure–flow indicators are objective markers of deglutitive function, which are altered in relation to ineffective swallowing. In adults, aspiration risk can be assessed through derivation of a swallow risk index (SRI), which is a formula combining 4 pharyngeal pressure–flow indicators relevant to aspiration (11–13). Also, AIM analysis has high intrarater and interrater reproducibility for derivation of pharyngeal pressure–flow variables and the SRI (14) and may therefore have clinical utility as an objective, reliable, nonradiological method for assessing deglutitive function in children. The purpose of the present study was to determine whether this new methodology is similarly applicable to children with dysphagia referred for videofluoroscopic assessment of swallowing.
The present prospective study included 20 paediatric patients with dysphagia (mean age 6 years, range 5 months to 13.4 years) who were referred to our dysphagia research program for a videomanometry study of the pharynx and oesophagus for a>2-year period (University Hospital Leuven, Belgium). Any child younger than 18 years of age referred for swallow assessment presenting with 1 of the following severe signs of dysphagia could be included in the study: coughing, choking, obstruction and/or apnoea during mealtimes, food refusal, nasal regurgitation, inadequate control of oral secretions, and insufficient suck–swallow–breathe coordination. Children on ventilation or who were oxygen dependent at the time of referral were excluded. Underlying diseases/conditions were identified through a review of medical records. The majority of patients had a neurological history (Fig. 1). Neurological diagnoses (N = 12) were cerebral palsy (10/12), developmental delay (1/12), and slowly progressive ataxia with cerebellar atrophy (1/12). Gastrointestinal disorders (N = 4) were oesophageal motility disorders (3/4) and gastro-oesophageal reflux disease (1/4). Two children had a congenital heart defect (ventricular/atrial septal defect), and 2 children presented with an ear, nose and throat pathology (cleft palate [1/2] and laryngomalacia [1/2]). Patients presented with a variety of clinical signs such as gagging, food refusal, nausea, noisy breathing, vomiting, crying, choking during meals with coughing and apnoeic episodes, suboptimal weight gain, frequent coughing, frequent respiratory infections, and difficulty managing secretions. None of the patients had previous documentation of deglutitive aspiration at the time of referral.
Written informed consent was obtained before the study and signed by the primary caregiver of the child. The study protocol was approved by the research ethics committee of the University Hospital Leuven (ML 3672).
All fluoroscopy studies were performed in the Radiology Department, University Hospital Leuven. Studies were performed using a 2.5-mm-diameter solid-state manometry and impedance catheter incorporating either twenty-five 1-cm-spaced pressure sensors and twelve 2-cm-long impedance segments or thirty-six 1-cm-spaced pressure sensors and sixteen 2-cm-long impedance segments (Unisensor USA Inc, Portsmouth, NH). Subjects were intubated with topical anaesthesia (lignocaine gel) used to reduce discomfort, and the catheter was positioned with sensors straddling the entire pharyngo-oesophageal segment (velopharynx to proximal oesophagus). Pressure and impedance data were acquired (upright position) at 20 Hz (Solar GI acquisition system, MMS, Enschede, the Netherlands). As per routine clinical fluoroscopy, 1 to 10 mL of liquid, semisolid and solid test boluses (dependent on age and tolerance) were administered orally via syringe. Because of low number of semisolid and solid boluses across our study cohort, only liquid boluses were included for further analysis.
In the analysis, swallows were stratified either by aspiration/penetration based on a swallow by swallow analysis or by global aspiration by the patient. A global aspirator is defined as a patient who aspirated on any 1 of the swallows during the study, either on a primary or clearing swallow or on any liquid, semisolid or solid bolus throughout the radiological examination. In the present study only liquid primary swallows were used for the validation of AIM versus videofluoroscopy. All bolus stock contained 1% NaCl to improve bolus conductivity. Video loops of the fluoroscopy images of swallows were simultaneously acquired (25 frames per second). The manometry and impedance catheter was on average in situ for 30 minutes, and the patient was extubated immediately on determination of the procedure. No adverse events occurred, and patient tolerance of the procedure was good to excellent.
Fluoroscopic Assessment of Aspiration–Penetration
Fluoroscopic images were scored (NR) for residue and the occurrence of aspiration–penetration blinded to the manometric findings and to the performed radiological procedure. Swallows were assessed for the presence of aspiration–penetration using a validated 8-point score (15), influenced primarily with the depth to which material passes in the airway and with whether or not material entering the airway is expelled during the swallow sequence (score 1 = no aspiration, 2–5 = penetration, 6–8 = aspiration). Swallows were also assessed dichotomously for the presence or absence of postswallow residue in the valleculae, piriform sinus, and/or posterior pharyngeal wall.
Manometry and impedance recordings were correlated precisely in time with fluoroscopic images and analysed to derive 4 different pharyngeal pressure–flow variables indicative of timing and duration of maximal bolus flow, pressure during maximal bolus flow, and pharyngeal contractile pressure. The derivation of variables has been previously described (11–14) and is summarised below.
Raw manometric and impedance data for each fluoroscopically observed swallow were exported from the recording system in ASCII text format and then analysed by a separate computer using MATLAB (version 184.108.40.2069; MathWorks Inc, Natick, MA). A new method of impedance analysis was developed that analysed the shape of the impedance waveform, rather than the magnitude of impedance change (11). To do this reliably, the raw impedance data were standardised to the median impedance, presented therefore as median standardised units rather than ohms.
Pharyngeal Pressure–Flow Variables
From the pressure colour isocontour plot, 2 regions of interest (ROIs) were defined relative to swallow onset (defined by the initiation of either UES relaxation or orad movement of the UES high-pressure zone).
The first ROI encompassed the spatial region from velopharynx to the proximal margin of the UES high-pressure zone. The timings of the pharyngeal nadir impedance (NadImp) and peak pressure (PeakP) were determined (Fig. 2B) along the first ROI. The average pressure at NadImp (PNadImp), average PeakP and average time delay from NadImp to PeakP (TNadImp-PeakP) were then calculated (Fig. 2C).
The second ROI encompassed the pharyngeal stripping wave from tongue base to proximal margin of the UES high-pressure zone (Fig. 2A and D). The maximum impedances within the second ROI were measured (Fig. 2E). An impedance versus cumulative time plot was derived (Fig. 2F); this plot was then mathematically described using third-order polynomial equation (the typical equation for a curve with 1 inflexion). The cumulative time of the inflexion point of a smoothed best-fit curve was used to objectively calculate the flow interval (Fig. 2F).
UES Relaxation Variables
The third ROI encompassed the UES high-pressure zone. UES relaxation characteristics were measured using the established method of Ghosh et al (16) that objectively calculated UES relaxation interval (UES-RI), the UES nadir relaxation pressure, the UES median intrabolus pressure (UES-IBP), and the UES resistance (calculated as UES-IBP/UES-RI). The UES NadImp correlates with UES opening diameter (17), and the UES PNadImp measures UES intrabolus pressure.
Swallow Risk Index
An SRI was derived by the following formula:
The above-mentioned formula was previously developed based on an iterative evaluation of the multiple pressure and impedance variables to identify motor function associated with aspiration of liquid boluses (12).
Postswallow residue was determined using the integrated ratio of nadir impedance to impedance (iNadImp/Imp ratio) that relates postswallow impedance to the impedance during bolus passage (18) and is elevated with large postswallow residues.
Nonparametric grouped data were presented as medians (interquartile range) or as mean ± standard deviation and compared using the Mann-Whitney rank sum test. For multiple comparisons Kruskal-Wallis ANOVA on ranks with pairwise multiple analysis procedures (Dunn method) was used. Correlation was determined using a Spearman rank-order correlation.
A total of 58 swallows were evaluated with the 2 modalities of fluoroscopy and AIM. Each patient received a number of boluses with a consistent volume depending on their individual age and tolerance. Bolus volumes administered to the mouth varied from 1 to 10 mL (mean 3.3 ± 2.7 mL). Half of the boluses administered were <2 mL (28 swallows).
Changes in Swallow Variables in Relation to Fluoroscopy Findings
Aspiration–penetration on liquid swallows was observed during a total of 9 swallows in 5 patients. One patient aspirated on a semisolid bolus. The median [interquartile range] aspiration score was 8 [8, 8] for these aspiration-associated swallows, indicating silent aspiration.
Patients with aspiration–penetration (N = 12) had a higher SRI and a higher integrated NadImp/Imp value indicative of postswallow residue compared with patients with no aspiration or penetration. All other swallow variables were not significantly different in relation to the presence/absence of aspiration. Data are presented in Table 1. Both longer flow interval and higher SRI correlated with higher aspiration scores (Table 2). Example tracings and calculations from a patient with deglutitive aspiration are provided in Figure 2A–F.
Patients with global aspiration (N = 6) (aspiration on liquids and/or semisolids and solids) had a higher SRI, a longer flow interval, and increased UES PNadImp than those without aspiration (Table 1). A trend towards higher pressure at nadirImp was also apparent (Table 1). All 3 indicators—SRI, flow interval, and UES PNadImp—correlated with higher aspiration scores. All other swallow variables were not significantly different in relation to the presence/absence of aspiration (Table 1).
Four patients presented with bolus residue after the swallow. In these patients, a trend was found towards a higher integrated NadImp in case of bolus residue after clearance failure (P = 0.096).
In the present pilot study, pharyngeal AIM analysis was applied to a cohort of children with suspected aspiration referred for videofluoroscopy. We evaluated the SRI that is based on the objective calculation of 4 pharyngeal pressure–flow variables. As has been previously demonstrated in adults, the SRI was elevated in relation to the occurrence of aspiration. This new methodology therefore may have clinical potential to identify individual patients at deglutitive aspiration risk in addition to or without use of fluoroscopy. This catheter-based method differs from a radiological approach because it allows quantification of multiple aspects of swallow function and sets substantial less limits to the duration of the examination, which clinically may improve the accuracy and realistic reflection of the child's swallowing potential.
The AIM analysis approach contrasts with the standard approach that evaluates impedance findings separately from pressure and defines periods of time during which impedance is above or below a certain cutoff value to calculate 1 measure (bolus clearance time). AIM analysis improves the analysis of impedance–manometry recordings by extracting objective readings of swallow function variables and combining them into the SRI. Because the SRI takes into account these different measures of function, it delivers a more accurate assessment of aspiration risk. Recognition of particular patterns of impairment of pressure–flow variables should allow a relatively specific diagnosis of varying mechanical dysfunctions that result in aspiration. From such analysis, it may be possible to devise well-targeted therapeutic interventions.
In children, as has already been shown in adults (12,13), we observed that UES relaxation pressure variables (nadir UES pressure, intrabolus pressure, and UES resistance) (15) were not significantly altered in relation to the presence of aspiration. Our impedance-based indicator of UES PNadImp, reflecting the pressure during maximal bolus flow through the UES, was increased in those patients who aspirated. This is an interesting finding because it indicates that the impedance-based pressure indicator picks up a subtle change in UES response to bolus flow in case of aspiration, not detected by pressure measurement alone (UES intrabolus pressure). The fact that this UES pressure–flow indicator allows identification of subtle differences in UES function may clinically be valuable, given that some interventions for aspiration, such as UES myotomy and botulinum toxin injection, are aimed at weakening the UES pressure (19). This integrated approach of pressure and flow analysis may therefore be particularly useful in assessing postintervention outcomes.
In infants, a noisy wet upper airway sound after a swallow or increasing noisiness during the course of feeding is a well-known clinical indication of swallow dysfunction and increased aspiration risk (20). If the child's breathing becomes noisier as the feeding progresses and the sound is originating in the pharynx, there may be inadequate pharyngeal clearance or UES obstruction leading to pooling of bolus residue in the pharynx (21). Aspiration can then occur as the bolus is inhaled or passively falling into the open airway after the swallow. Using our AIM methodology, postswallow residue was shown to be reliably detected in adults by means of the iNadImp/Imp ratio (18). In our paediatric population, this indicator was significantly elevated in patients with aspiration/penetration compared with patients without. This indicates that children with aspiration/penetration are more likely to have postswallow residue. In patients with aspiration only, the Nadimp/imp value was also elevated but did not reach statistical significance probably because of the small sample size.
Although it has been widely demonstrated that volume swallowed can influence individual functional indicators, such as PeakPs and UES-RI (16,22), our previous studies of adult patients with dysphagia showed no significant volume effects on the SRI (12,13). This is particularly encouraging of potential utility in paediatric patients, in whom the volume administered during swallow testing is difficult to control and, even if a standardised volume is administered to the mouth, it may nevertheless take several swallows to consume. In the present paediatric study, we were unable to assess volume effect within each individual patient because patients were given a tailored volume according to their own clinical capacity and in a consistent way throughout their examination. Our ongoing paediatric research aims to address this volume question.
The fact that the SRI is elevated in relation to aspiration in the present pilot study supports translation of this new methodology to the paediatric population and therefore warrants further investigation by way of outcome studies to determine whether, for example, SRI predicts clinical deterioration and efficacy of interventions. The recent development of purpose-designed software that can reliably perform AIM analysis (14) will make such investigations easier to undertake in the future.
In conclusion, we present novel pilot findings in a cohort of paediatric patients with predominantly neurological problems who were referred for investigation of suspected aspiration. These data show that combined high-resolution solid-state manometry and impedance recordings that are objectively analysed using AIM analysis can derive robust pressure–flow variables that are altered in relation to pathology. More important, a SRI can be derived through the combination of these pressure–flow variables and used to predict circumstances when aspiration is likely. Based on these data, we believe that pharyngeal AIM analysis is clinically applicable for assessing deglutitive dysfunction and aspiration risk in paediatric patients with dysphagia.
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Keywords:© 2014 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology,
deglutition disorders; diagnosis; electric impedance; manometry; respiratory aspiration