What Is Known
- Bolus volume impacts high-resolution impedance manometry swallow metrics.
What Is New
- Piecemeal deglutition that breaks up an orally administered bolus into smaller more manageable volumes should be recognized in high-resolution impedance manometry assessments.
- A methodology is described for swallow selection from a piecemeal deglutition sequence for analysis of high-resolution impedance manometry assessments.
High-resolution impedance manometry (HRIM) provides objective pressure and integrated bolus flow assessment of pediatric swallowing (1–3). To date, analysis of HRIM assessments has relied on single swallow selection following oral administration of a bolus, even when a bolus is swallowed in multiple portions. Piecemeal deglutition (PD), defined as swallowing of 1 single bolus in 2 or more portions to empty the oral cavity (4), is a common feature of pediatric swallowing. While pediatric PD research in infants >6 months is limited, it is expected that PD occurs normally when the swallow mechanism is challenged with a larger than optimal bolus volume (5); however, in oropharyngeal dysphagia (OPD), PD may even occur for boluses of optimal volume and is, therefore, suggestive of impairment (6,7).
The healthy swallowing mechanism modulates to accommodate bolus volumes and this is reflected by changes to pressure flow metrics detected from HRIM methods. Incremental increases in volume have shown larger velopharyngeal to tongue base occlusive pressures for propulsion of a bigger bolus; higher hypopharyngeal intrabolus pressure (hIBP); earlier upper esophageal sphincter (UES) relaxation; and earlier and wider UES opening (8–12). Therefore, as PD naturally distributes the administered volume over several piecemeal swallows, it follows that pressure flow swallow metrics will in turn be altered.
Manometry can be performed in infants and young children and enables clear observation of oropharyngeal swallowing motor patterns (1–3,13–15). It is critical for assessors to differentiate saliva from bolus containing swallows when selecting for analysis, as only bolus swallows will allow accurate assessment of a child's ability to manage foods and liquids. This can be achieved using impedance measures that capture bolus flow (16), thus avoiding the constraints inherent with use of ionizing radiation (17). Therefore, this exploratory study aimed to define a swallow selection methodology that best captures pharyngeal and UES function in infants and children aged 5 months to 4 years where PD is a feature of the HRIM recording; characterize PD patterns in relation to age; and determine the effect of PD patterns on swallow function variables. We hypothesized that single swallow selection of the first swallow in a piecemeal sequence may incorrectly represent a child's bolus swallow function measures.
All investigations were performed in the Department of Paediatric Surgery at The Royal Children's Hospital, Melbourne, Australia. The institutional Human Research Ethics Committee approved the study protocol in accordance with the Australian Paediatric Research Ethics and Governance Network (HREC 35089A). Informed consent was obtained from all participants’ primary caregivers before commencing measurements. Participants underwent investigations in the presence of a research nurse, parent(s), pediatric surgeon, and scientist/speech pathologist. The HRIM recordings from each child were retrospectively analyzed for the purpose of this study.
HRIM procedures had been previously performed as part of a research study primarily aimed at investigating esophageal motility in children with type IIIb esophageal atresia (EA). In these patients pharyngeal swallowing was considered “asymptomatic” on clinical grounds (no history of clinical symptoms, assessment or interventions for OPD). Preoperatively, the majority of patients underwent laryngo-tracheo-bronchoscopy (LTB) to document vocal cord mobility, confirm the presence and position of the trachea-esophageal fistula associated with this type of EA, and to exclude laryngeal cleft. In those patients that do not undergo preoperative LTB, it is routine care at this center for an investigation to be arranged postoperatively if patients demonstrate respiratory symptoms. None of our cohort had laryngeal cleft, vocal cord paralysis or demonstrated symptoms to warrant LTB postoperatively.
For the purpose of our analysis, the participants were grouped by age: Group 1 (5–11 months of age) and Group 2 (1–4 years of age), as 1 year of age optimally defined developmental transition from infant to child swallowing behaviors (18,19).
The HRIM recordings were acquired using an 8 French high-resolution, solid-state catheter incorporating 32 pressure sensors and 16 adjoining impedance segments (32P16Z) (Unisensor AG catheter, Attikon, Switzerland). The pressure sensors detect the sequence of pressure changes associated with swallow musculature contractions and the impedance electrodes record flow of ingested food/fluid.
The catheter was positioned transnasally, straddling the entire pharyngo-esophageal segment. Where tolerated, lignocaine spray (5%) had been applied to the entrance of the nose and a water-based lubricant was used to assist with catheter placement. The pressure-impedance data were acquired at 20 samples per second (Solar GI acquisition unit Medical Measurement Systems, Enschede, The Netherlands).
Boluses of 0.9% sodium chloride (saline) were used during the HRIM assessment. These boluses had been administered orally via a syringe and a consistent volume was given to each patient, ranging from 2 to 5 mL depending on patient age/size. The manometric “composite pharyngeal responses” (15) within a 15-second window were observed to define piecemeal patterns. This study presents integrated impedance with manometry data (Fig. 1).
Analysis of Pressure-Impedance Recordings
The HRIM recordings were retrospectively analyzed using the software platform AIMplot (courtesy T.O.), which is accessible online via a web-based portal called Swallow Gateway (Fig. 2). The entire HRIM study was exported as an ASCII file, which was then uploaded onto the website (swallowgateway.com). The impedance values are automatically transformed to their inverse product, admittance (admittance = 1/ohms; units in millisiemens, mS), providing a measure of bolus passage through the pharyngo-esophageal segment.
Once uploaded to Swallow Gateway, the study was navigated to select pharyngeal swallow sequences (up to a maximum of 5 swallows within a 15 second HRIM recording window) following bolus administration. PD was noted to define the swallow sequences. The largest admittance peak within the sequence specified the largest volume swallow, defined as the dominant swallow (see Fig. 1). The dominant swallow was used to set the admittance threshold at the reference point of UES closure (as defined by the onset of postrelaxation contraction of the UES) (Fig. 2C). Setting the admittance threshold at UES closure ensured that admittance values at and above this threshold were meaningful for that individual's (optimally conductive) bolus swallows. Consequently, admittance values above the threshold indicated true bolus passage with the assumption that bolus passage ceased by the time the UES had closed. Swallows with admittance values below this threshold were considered dry/secretion swallows, which were excluded from PD analysis.
PD patterns were defined according to the number of PD swallows in a sequence as follows: pattern A = 1–2 swallows; pattern B = 3 swallows; pattern C = 4–5 swallows. This definition allowed for homogenous group sizes for overall statistical comparison.
The bolus swallows in each PD sequence were individually selected and analyzed to derive swallow function variables that were averaged for each PD sequence. Additionally, the dominant swallow (as defined above) was highlighted so that it could be compared to the averaged data from each PD sequence. The swallow function variables calculated are described below.
Swallow Function Variables
All swallow function variables (SFV) are indicated in Figure 2. The velopharyngeal tongue base contractile integral (VCI) was based on the integral of pressures within the region of the velopharynx and tongue base during a swallow. Contractility of the pharyngeal stripping wave proximal to the UES was calculated as the pharyngeal peak pressure (Peak P), defined as the maximum contraction of the pharynx. Additionally, the UES post relaxation peak pressure (UES Peak P) was determined by the maximal peak pressure up to 1 second after relaxation offset. The distension-contraction latency of the whole pharynx (Ph DCL) was determined for the pharyngeal region proximal to the UES apogee position. This temporal metric defines the latency from maximum bolus distension to maximal pharyngeal contraction and is a marker of how well the bolus is propelled ahead of the pharyngeal stripping wave.
The maximum admittance estimates the area at the axial center, or most distended part, of the lumen during bolus transport (16). Hence, pharyngeal pressure measured at, and the relative timing of, maximum admittance provides an accurate measure of pharyngeal intrabolus distension and timing of maximum distension, respectively. For this study, the hypopharyngeal intrabolus pressure at maximum admittance, 1 cm above the UES, was used to define hIBP. The maximum luminal cross-sectional area within the UES, during bolus flow, was inferred based on the UES maximum admittance (UES Max Ad) (16,20).
The UES basal pressure (UES basal P) and UES relaxation pressure were determined using the e-sleeve method, based on the value and location of maximum axial UES pressure over time (21). The UES integrated relaxation pressure (UES IRP) was defined as the median of all lowest pressures (contiguous or non-contiguous) recorded over a 0.25-second period. The UES open time (UES OT) was defined by the period between the upstroke and down stroke inflexions of the UES admittance curve.
The data were investigated using SPSS (IBM Corp, released 2013, IBM Statistical Package for the Social Sciences [SPSS] Statistics for Windows, v 22.0 Armonk, NY: IBM Corp). Measurements were predominantly nonparametric; therefore, for all PD pattern comparisons Independent Sample Kruskall-Wallis Tests were conducted. A Bonferroni adjustment was manually applied for multiple pairwise comparisons. For age group comparisons, a Mann-Whitney U test was performed. Throughout, a P <0.05 indicated statistical significance.
Participants who took at least 3 swallows of a constant volume of at least 2 mL liquid were included for analysis. A total of 27 patients (19 boys, 8 girls) were included in this study. There were 13 patients in age Group 1 (median age 7 months, range 5–11 months) and 14 patients in age Group 2 (median age 18.5 months, range 13–41 months). All participants were receiving full oral diet without modification, with no clinical signs, symptoms or history of OPD. Overall, the prevailing PD pattern was pattern B (43.7%) followed by pattern A (35.6%), and pattern C (20.7%). Group 1 (infants) and Group 2 (children 1–4 years) showed a similar distribution of PD patterns (Figure, Supplemental Digital Content 1, http://links.lww.com/MPG/B439). There were, however, clear biomechanical differences between the age groups, consistent with a larger oral and pharyngeal chamber in the older children (Fig. 3).
Similar findings were noted when data based on the dominant swallow within the PD pattern type were compared with those from the average of the swallows. However, the dominant swallow data showed the greatest statistical confidences for age and PD pattern main effects and are therefore presented here (Fig. 3, Table 1).
The main age-related differences were greater UES distension diameter indicated by UES maximal admittance (Fig. 3B) and lower UES relaxation pressures (Fig. 3C), a longer distension-contraction latency (Fig. 3D) and higher hIBP (Table 1) among older children. Velopharyngeal to tongue base contractility pressures, hypopharyngeal peak pressure and UES basal and postrelaxation peak pressure were not affected by age group (Table 1).
The main differences for PD pattern type were a higher velopharyngeal contractility (Fig. 3A), wider UES distension diameter indicated by UES maximal admittance (Fig. 3B), longer UES opening time (Fig. 3E), lower UES relaxation pressures (Fig. 3C) and longer pharyngeal distension-contraction latency (Fig. 3D) for fewer swallows in a PD sequence. The hIBP, hypopharyngeal peak pressure, and UES basal and peak pressures were not affected by PD pattern (Table 1).
Our study aimed to determine whether PD impacts pressure flow metrics derived from HRIM assessments. Additionally, we intended to characterize patterns of PD during HRIM assessments in this pediatric cohort, asymptomatic of OPD. As ethical considerations protect healthy children from invasive testing, we evaluated recordings from a case series of children with uniform type IIIb EA who primarily underwent HRIM investigation for esophageal motility, but were without symptoms of OPD. We observed a prevalent 3 swallow piecemeal sequence across the cohort. Furthermore, PD pattern types were associated with differences in swallowing biomechanics across the cohort and these changes were consistent with larger bolus volumes swallowed when fewer piecemeal swallows occurred. Age-group specific differences in pressure flow metrics were evident between infants and children in this cohort; these variants were consistent with older children having a larger pharyngeal chamber. Additionally, we demonstrated a clinically relevant swallow selection method whereby the dominant swallow is identified in a PD sequence and, according to this cohort, provides sufficiently meaningful swallow function data.
The ability to discriminate between saliva and bolus swallows is paramount during manometric swallow assessments. As infants and young children seldom swallow on cue, swallow markers may not reflect the dominant swallow. Our results confirm our hypothesis that selection of the first swallow in a sequence may provide inaccurate indications of swallow function. Our findings suggest that assessors can reliably identify the dominant swallow, defined as the largest bolus swallow based on the admittance curves and objective admittance values in a PD sequence (see Figs. 1 and 2B), thereby optimizing the analysis process.
While normative data are lacking in age matched pediatric cohorts, it is likely that larger than normal boluses will naturally elicit a PD sequence. In newborns and very young infants a volumetric dose-response has been reported in the pharynx whereby an increase in pharyngeal swallows occurred with increases in volumes (0.1, 0.3, 0.5 mL) (13). This work by Jadcherla et al has also explored the newborn/infant pharyngeal swallow reflex and volume modulated responses in relation to respiratory patterns, which indicate the intricate processes of airway protection during deglutition (14,15). On the whole, pediatric PD literature is, however, limited; to our knowledge this is the first paper to report PD in the context of HRIM assessments in children.
It has previously been shown that natural swallow volume during suckle feeding per swallow doubles to 0.4 ml in the first month of life (22). A separate study by McGowan et al, however, reported volumes of 0.26 ml in a cohort of children during suck swallowing at 12 months of age (23). To our knowledge, single bolus volumes to indicate an upper limit tolerated (dysphagia limit) before multiple swallowing is required (24) has not been established in pediatric swallowing, however, would help to differentiate physiologically normal PD from the multiple swallowing seen in the context of OPD. To date, PD has been described as a feature of OPD, whereby piecemeal or multiple swallowing indicates impaired lingual strength/movement, and pharyngeal swallow impairment (6,7). Additionally, in the absence of obvious muscle weakness amongst patients, PD is clinically noted for possible swallow fear (phagophobia), hypersensitivity to large boluses, or retention of a suckle pattern due to developmental delay or disorders (6,7).
It is important to note the volumes given in this study were offered according to the primary investigation of esophageal motility, which aimed to challenge the compliance of the esophagus following EA repair. The HRIM recordings have opportunistically been analyzed as the pharyngeal segment was captured in this cohort of children asymptomatic of OPD, who would not otherwise have undergone pharyngeal manometry assessment. Therefore, our study demonstrates that infants and children receiving a single oral bolus (2–5 mL) during HRIM assessment usually consume the bolus over 3 swallows (PD pattern B). We anticipated that children older than 12 months would show fewer PD swallows to clear the bolus from the oral cavity; however, the PD pattern distribution did not differ from that of infants, suggesting that PD is a fairly ubiquitous swallowing behavior in both infants and children undergoing HRIM assessment.
PD pattern A (1–2 swallows) was associated with differences in UES relaxation pressure, pharyngeal flow timing and velopharyngeal contractility when compared to patterns B and C, which is consistent with previous reports that show a larger bolus volume impacts these swallow function variables (12,25). Velopharyngeal contractility and UES opening diameter were especially affected; both showing the greatest differences between PD pattern subtypes (Fig. 3A and B). Importantly, without consideration for PD during HRIM analysis, a low UES admittance value could be misinterpreted as impaired UES opening when in fact it is caused by the reduced bolus volume associated with PD.
We note that UES integrated relaxation pressure was inconsistent between averaged and dominant swallow data; it was reduced for averaged PD data but increased for dominant swallow data. This finding is because dominant swallows provide a larger bolus volume for analysis and; therefore, the UES relaxation pressures are higher when compared to the averaged results. Nevertheless, we would advocate for selection of the dominant swallow analysis for interpretation of UES IRP due to biomechanical plausibility and improved reliability of results from a larger bolus volume.
The pediatric age-related differences in some swallow function variables follow expectations for a relatively larger pharyngeal chamber amongst older children. For example, hypopharyngeal intrabolus pressure was higher, UES relaxation pressures were lower, UES opening diameter was wider (higher admittance) and distension-contraction latency was longer amongst older children compared to infants.
We acknowledge the limitations of this study. Results are based on children with EA and, while it is established that esophageal peristalsis is disrupted, the impact on oropharyngeal swallowing is less clear (26,27). These children were considered suitable for this initial description of PD as pharyngeal swallow patterns were adventitiously captured during their investigations. A criterion standard approach to exclude OPD (barium radiology or FEES) was not possible due to ethical constraints; however, the attending doctor and parent reports confirmed each participant was asymptomatic of OPD. We propose that the data presented here are a close representation of unimpaired oropharyngeal swallowing in young children, in a population that ethically could not be assessed for pharyngeal function using the HRIM methodology. While saline may be unfamiliar to a child during the HRIM assessment, saline swallowing is standard procedure for HRIM investigations as it is highly conductive and optimizes impedance recordings. Our retrospective analysis grouped the volumes given to participants (2–5 mL) as the sample size (n = 27) did not lend to statistical exploration of individual volumes. Bolus volume control in pediatric oropharyngeal swallowing is challenging due to anterior spillage and refusal; however, prospective studies with larger cohort sizes will need to address the lack of standard volume comparisons. Description of swallow patterns from a control group not undergoing an HRIM investigation may provide further details on the natural piecemeal patterns in this age group; however, this was not ethically feasible or intended for this study.
Overall, this exploratory study demonstrates that PD patterns impact pressure flow swallow metrics. We have highlighted key differences in the swallowing biomechanics between infants and children and in relation to PD pattern. All HRIM swallow assessments should note and adjust for PD to accurately capture an individual's swallow function. We propose that the dominant swallow within a piecemeal sequence provides a meaningful analysis of swallowing function and is simpler to perform than averaged PD data. The discrimination of the dominant swallow requires that impedance is recorded. We propose the dominant swallow data from a piecemeal sequence should always be interpreted in the context of the overall PD pattern observed. The causes for PD will depend on the clinical presentation and age for each patient. Therefore, to confirm these findings and build pediatric reference ranges, future studies should record PD patterns in esophageal atresia children with and without OPD, as well as other pediatric OPD cohorts.
1. Rommel N, Omari T, Selleslagh M, et al. High-resolution manometry combined with impedance measurements discriminates the cause of dysphagia in children. Eur J Pediatr
2. Ferris L, Rommel N, Doeltgen S, et al. Pressure-flow analysis for the assessment of pediatric oropharyngeal dysphagia. J Pediatr
3. Singendonk M, Rommel N, Omari T, et al. Upper gastrointestinal motility: prenatal development and problems in infancy. Nat Rev Gastroenterol Hepatol
4. Logemann JA. Evaluation and Treatment of Swallowing Disorders. 2nd ed.Austin, TX: Pro-Ed Inc; 1998.
5. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol
6. van den Engel-Hoek L, Erasmus CE, van Hulst KCM, et al. Children with central and peripheral neurologic disorders have distinguishable patterns of dysphagia on videofluoroscopic swallow study. J Child Neurol
7. Benfer K, Weir K, Bell KL, et al. Clinical signs suggestive of pharyngeal dysphagia in preschool children with cerebral palsy. Res Dev Disabil
8. Cook IJ, Dodds WJ, Dantas RO, et al. Opening mechanism of the human upper esophageal sphincter. Am J Physiol
2016; 257 (5 pt 1):G748–G759.
9. Dantas RO, Kern MK, Massey BT, et al. Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol
1990; 257 (5 pt 1):G675–G681.
10. Cook IJ, Dodds WJ, Dantas RO, et al. Timing of videofluoroscopic, manometric events, and bolus transit during the oral and pharyngeal phases of swallowing. Dysphagia
11. Lazarus CL, Logemann JA, Rademaker AW, et al. Effects of bolus volume, viscosity, and repeated swallows in nonstroke subjects and stroke patients. Arch Phys Med Rehabil
12. Ferris L, Schar M, McCall L, et al. Characterization of swallow modulation in response to bolus volume in healthy subjects accounting for catheter diameter. Laryngoscope
13. Jadcherla SR, Stoner E, Gupta A, et al. Evaluation and management of neonatal dysphagia: Impact of pharyngoesophageal motility studies and multidisciplinary feeding strategy. J Pediatr Gastroenterol Nutr
14. Jadcherla SR. Advances with neonatal aerodigestive science in the pursuit of safe swallowing in infants: Invited Review. Dysphagia
15. Hasenstab KA, Sitaram S, Lang I, et al. Maturation modulates pharyngeal-stimulus provoked pharyngeal and respiratory rhythms in human infants. Dysphagia
16. Cock C, Omari T. Current gastroenterology reports diagnosis of swallowing disorders: how we interpret pharyngeal manometry. Current Gastroenterology Reports
17. Arvedson JC, Lefton-Greif MA. Instrumental assessment of pediatric dysphagia. Semin Speech Lang
18. Coppens CH, van den Engel-Hoek L, Scharbatke H, et al. Dysphagia in children with repaired oesophageal atresia. Eur J Pediatr
19. Arvedson JC, Rogers B, Brodsky L. Arvedson JC, Brodsky L. Anatomy, embryology and physiology. Pediatric Swallowing and Feeding Assessment and Management
. San Diego: Singular Publishing Group; 1993. 5–51.
20. Cock C, Besanko L, Kritas S, et al. Maximum upper esophageal sphincter (UES) admittance: a non-specific marker of UES dysfunction. Neurogastroenterol Motil
21. Ghosh SK, Pandolfino JE, Zhang Q, et al. Deglutitive upper esophageal sphincter relaxation: a study of 75 volunteer subjects using solid-state high-resolution manometry. Am J Physiol Gastrointest Liver Physiol
22. Qureshi M a, Vice FL, Taciak VL, et al. Changes in rhythmic suckle feeding patterns in term infants in the first month of life. Dev Med Child Neurol
23. McGowan JS, Marsh RR, Fowler SM, et al. Developmental patterns of normal nutritive sucking in infants. Dev Med Child Neurol
24. Ertekin C, Aydoğdu I, Yüceyar N. Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders. J Neurol Neurosurg Psychiatry
25. Cock C, Jones C, Hammer M, et al. Modulation of upper esophageal sphincter (UES) relaxation and opening during volume swallowing. Dyphagia
26. Mahoney L, Rosen R. Feeding difficulties in children with esophageal atresia. Paediatr Respir Rev
27. Rommel N, Rayan M, Scheerans C, et al. The Potential benefits of applying recent advances in esophageal motility testing in patients with esophageal atresia. Front Pediatr