Videofluoroscopic study of swallowing
VFSS is considered the gold standard clinical assessment of swallowing in both children and adults, with the advantage that it directly visualizes all phases of swallowing . Despite its availability and popularity, interpretation of VFSS findings, in many cases, remains largely subjective . In the last 2 years, a number of studies have challenged subjective interpretation of VFSS findings.
The widely used Penetration-Aspiration Scale  is applied to videofluoroscopic imaging studies to grade airway violation during swallowing. It was critically reviewed by Steele and Grace-Martin  in terms of its clinical and research use. The Penetration-Aspiration Scale is used across the lifespan in VFSS  and has also been adapted for functional endoscopic evaluation of swallowing (FEES) [12–15]. The authors question using the scale as ‘ordinal’ in research data analysis and make suggestions for alternative ways to code or interpret the scale.
By establishing quantitative timing and displacement VFSS measures for healthy adults, Leonard et al.  and Kendall et al.  have shown its great clinical potential for improving accuracy of physiological diagnostics to aid decision-making in swallowing management. In the United States, Lee et al.  reported subjective measures of hyoid elevation, pharyngeal constriction ratio and pharyngo-oesophageal segment opening to be highly inconsistent among raters with accuracy ranging from 45 to 72%, compared with objective measures of adult VFSS. Further, they emphasize the importance of objective analysis of VFSS measures to standardize its interpretation, by revealing moderate overall inter-rater reliability of subjective VFSS measures. Meanwhile, in New Zealand, The University of Auckland Swallowing Laboratory explored competency development in obtaining objective measures of adult VFSS . They found that speech and language therapists could learn and rate objective VFSS measures within a feasible time frame, irrespective of their level of experience, which is promising for its potential to offer reproducible objective measures for specific standardized care . These findings are relevant and likely to be transferable to paediatric populations.
Objective quantifiable VFSS measures of children have been widely explored in the research arena in the recent past. In 2015, Gosa et al.  explored 15 objective temporal and physiologic measures of VFSS in children and found them all to be reliably measured. Henderson et al.  explored the feasibility of obtaining objective measures of timing and displacement in a paediatric VFSS clinic. They found that feasible and reproducible measures could be obtained by adopting a protocol, recording at an increased frame rate for short bursts, which overall did not increase radiation dose or exposure time. Sales et al. [21▪▪]describe a quantitative and qualitative temporal analysis of oropharyngeal swallowing in children with Down syndrome. Six qualitative binary parameters with two quantitative parameters were described in oral and pharyngeal phases of swallowing. Qualitative measures (oral incoordination, labial sphincter sealing incompetence, oral residue, posterior oral spillage, laryngo-tracheal penetration and laryngo-tracheal aspiration) were marked ‘binary’, as either present or absent, whereas pharyngeal transit time and total oral transit time were analyzed using a specific software [21▪▪]. This study is identified as the first to analyze objective temporal measures of swallowing in children with Down syndrome, recommending further studies with larger samples for quantitative analysis of swallowing in this clinical population.
Hyoid displacement plays an important role in airway protection during swallowing. Reduced hyoid displacement is associated with increased risk of residue and aspiration in adults . However, it has not been studied extensively in paediatrics. In a multicentre collaboration, Riley et al. [23▪▪] explored feasibility of measuring positioning and displacement of hyoid bone during swallowing in paediatric VFSS. They found visibility of hyoid bone increased with age, and was rarely visible in infants less than 9 months. This preliminary study is the first to explore objective hyoid measurements in children and leads to opportunities for further understanding of the role of the hyoid in the developing child.
Further work is required assessing training requirements and reliability of quantitative VFSS measures in children as well as building an understanding of swallowing physiological patterns across ages, severity profiles and cause (Fig. 2).
Modified barium swallow impairment profile
In 2018, Lefton-Greif et al. [24▪▪] reported the Modified Barium Swallow Impairment Profile (MBSImP) for bottle-fed children. The MBSImP  is a standardized tool for systematic interpretation of adult VFSS images. The paediatric version of the MBSImP includes components of bolus flow and physiologic movements of oropharyngeal structures during swallowing, which were identified by clinical experts, as essential for functional, efficient and well-tolerated swallowing in bottle-fed infants. MBSImP was used as the conceptual assessment tool to identify and quantify swallowing impairment. The authors tested inter-rater reliability, achieving 80% reliability by all the raters after completing three training–testing sessions. MBSImP for bottle-fed children offers clinicians working in paediatric dysphagia, a reliable systematic observation and criterion-based scoring of the swallowing mechanism.
Ultrasound, with the advantage of not exposing infants to ionizing radiation, has future potential as a noninvasive method of assessing swallowing physiology. In 2017, Remijn et al.  studied the oral stage of swallowing in children, aiming to describe the process of mastication. They explored the feasibility of the Mastication Observation and Evaluation tool, using dynamic ultrasound and 3D kinematic measures of masticatory skills in children with cerebral palsy, compared with typically developing children. The researchers first introduced this tool in 2014 , and then explored the measurement of mandibular movements in adults in 2016. In this most recent study, they used video-recorded ultrasound to measure horizontal and vertical movements of tongue and 3D kinematics to measure horizontal, vertical and anterior mandibular movements. Both 3D kinematics and ultrasound measures were capable of successfully differentiating disordered from healthy mastication in terms of frequency and timing of movements and duration of chewing cycles. The authors conclude that these objective ultrasound measures of tongue movements and timing measures could complement the Mastication Observation and Evaluation findings clinically. However, the need for specialized equipment and intensive training to administer and interpret ultrasound findings may restrict its practical clinical use among speech and language therapists [28▪].
PRESSURE FLOW AND IMPEDANCE
Manometry is a valid measure of pharyngeal and oesophageal pressures across time during swallowing. In adults, manometry measures are beneficial in planning surgical interventions, such as candidacy for cricopharyngeal myotomy . High-resolution pharyngo-oesophageal manometry with impedance has gained popularity in the last decade, providing vital information on bolus pressure and flow in pharyngeal and oesophageal phases of swallowing.
This year, Singendonk et al. [30▪]trialled a novel approach by combining pressure and impedance measures to evaluate oesophageal motility in children with achalasia. In this study, high-resolution oesophageal manometry was administered to children with achalasia and children without an oesophageal motility disorder using a standardized protocol. Measures included three oesophageal junction parameters: integrated relaxation pressure (IRP), bolus flow time (BFT) and bolus presence time (BPT). In achalasia, significantly lower BPT and BFT values were reported, compared with children without motility disorders. No significant differences were observed in BPT and BFT of treated and untreated groups of achalasia, suggesting that children may still exhibit persisting symptoms postdilatation therapy. In this study, selected oesophageal junction parameters successfully indicate oesophageal dysmotility in children with achalasia and it could be developed further for diagnosing a range of motility disorders as well as guiding decision-making and measuring efficacy of treatments (Fig. 3).
Pharyngeal manometry is a ‘hot topic’ across the lifespan. In 2018, Hasenstab et al. studied how maturation affects respiratory, pharyngeal and oesophageal aerodigestive rhythms during multiple pharyngeal swallow sequences. Preterm infants were studied longitudinally (for 4 weeks) to determine the effect on maturation and pharyngeal stimulus volume on multiple swallow response rhythms and respiratory characteristics. Pharyngo-oesophageal manometry results were analyzed to identify and describe pharyngeal swallow responses (PSR), by calculating frequency of multiple PSR for each participant. Further, multiple PSR were analyzed to calculate the number of pharyngeal peaks, pharyngeal frequency and stability. They report decreases in the number of pharyngeal peaks and pharyngeal peak duration, as infants advance in maturation. These findings expand our understanding of how preterm infants achieve stability in swallowing over the time, while maintaining airway protection. Pharyngeal manometry is likely to be seen more often in paediatric swallowing assessment in coming years.
It is well known that airway protection during swallowing is essential for survival. Neurological maturation and development is complex and therefore coordination of breathing, sucking and swallowing in preterm infants has been extensively studied . Hasenstab et al. used respiratory inductance plethysmography and nasal airflow thermistor readings alongside their manometry measures. Respiratory measures included: prevalence of deglutition apnoea, duration of deglutition apnoea, respiratory response latency, respiratory response duration and total respiratory rhythm change duration. Duration of deglutition apnoea significantly decreased with maturation. Moreover, their findings reflect similarity in findings of the literature, by suggesting that maturation modifies respiratory adaptive behaviours [33,34]. Authors acknowledge this study to be the first to investigate respiratory and pharyngeal characteristics of PSR patterns in neonates. This may add to our understanding of swallowing–respiration coordination in premature infants. The feasibility of using airflow measures in the clinic to guide management decisions is yet to be established.
Acceptance of cervical auscultation as an instrumental assessment is controversial. Some researchers question the correlation between cervical auscultation sounds and physiology of swallowing [28▪]. Yet, objective acoustic measures for children have been widely studied and standardized over the years [35–37]. In 2013, Frakking et al.  proved its potential as a diagnostic test to identify risk of oropharyngeal aspiration in children. However, they acknowledge that clinical significance of acoustic swallowing measures could be limited, if not related to perceptual parameters in interpreting swallowing sounds. Taking their research further, Frakking et al. aimed to develop normative data of acoustic and perceptual profiles of swallow sounds for 4–36 months old children using digital cervical auscultation. They studied healthy children aged 4–36 months, who are within the transitional feeding period, as significant changes to anatomical maturity of oropharynx take place during this period . Swallowing-related laryngeal movements were video recorded and an acoustic software was used to analyze the correlating auditory feedback of the swallow sound. Three acoustic parameters were analyzed for food and liquid consistencies: swallow duration, peak frequency and peak intensity/amplitude. They found the mean duration of swallows was less than 1 s for all food consistencies in children, whereas thin fluids marked the highest peak frequency and peak amplitude mean. A significant positive correlation was reported between peak amplitudes and age; the swallow sounds become louder as children get older. This study adds the largest collection of normative data to the previously developed normative data for different paediatric age groups [35,40]. However, the study fails to provide reliability ratings or to compare the acoustic measures with physiological measures of swallowing to see which swallow sound represents which physiological event during swallowing in children. The authors suggest considering mean swallow duration (<1 s) as a marker to identify healthy swallowing in children. This approach may drive future research directions, as it is noninvasive and less costly compared to existing instrumentations. Accessibility and ease of administration are advantages for clinical use.
FUTURE DIRECTIONS FOR INSTRUMENTAL ASSESSMENTS OF SWALLOWING
Standardizing quantitative and objective measures remains a priority in the field of paediatric instrumental swallowing assessment. Research should focus on clinically feasible, objective, quantitative reporting of physiological components of swallowing to facilitate medical and surgical decision-making for children with complaints of dysphagia. Considering the importance of VFSS as the gold standard visual-imaging assessment method and its technological development in the recent past, it is unacceptable to expose children to radiation only to confirm presence of aspiration. Rather, it should guide clinicians’ understanding of the underlying anatomical and physiological manifestations causing swallow dysfunction and aspiration. Establishing standard objective VFSS measures across developmental ages and different causes of swallowing should be a priority. As a nonradiological, yet invasive procedure, manometry with impedance has great potential to describe pharyngeal and oesophageal phases of swallowing, in terms of motility and pressure flow. FEES, another nonionizing invasive procedure, provides important information on pharyngo-laryngeal structure and function of airway protection during swallowing [28▪]. Even though no published scientific articles were found during the reviewed time period, it may prove worthwhile combining FEES with respiratory measures to describe swallowing–breathing coordination in young children. Development of specific and holistic management approaches for children, including novel noninvasive instrumental swallowing assessment, is needed.
The breadth of research into instrumental assessment of children is vast with a wide range of instrumental tools under investigation. Yet, there remains a lack of clarity on clinical feasibility and objective measures which facilitate medical decision-making in practice. Novel approaches to aid the quantification of swallowing physiology from the mouth, pharynx through to the oesophagus are emerging. Quantitative measures of VFSS, high-resolution manometry with impedance and ultrasound hold merit in the clinical setting.
We would like to thank Lisa McCall, Registered Nurse in the Gastroenterology Unit at Women's & Children's Hospital, Adelaide for Fig. 3.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
- ▪ of special interest
- ▪▪ of outstanding interest
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Keywords:Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved.
deglutition disorders; dysphagia; instrumental assessment; manometry; paediatric feeding; videofluoroscopic study of swallowing