Use of Pharyngeal High-Resolution Manometry to Evaluate Dysphagia in Adults with Motor Neurone Disease: A Scoping Review

Motor neurone disease (MND) is a life-limiting neurodegenerative condition characterised by the progressive decline of the motor neurones [1]. MND progresses rapidly, with average survival estimated at 2–4-year post-diagnosis [2]. The International Statistical Classification of Diseases and Related Health Problems (ICD-10) acknowledges four subtypes of MND [3]. Amyotrophic Lateral Sclerosis (ALS) is the most prevalent of the subtypes. The remaining subtypes include Progressive Bulbar Palsy, Progressive Muscular Atrophy and Primary Lateral Sclerosis [3]. At this point in time, there is no reversible treatment for what is typically a catastrophic collapse of a previously apparently normal functioning motor system. Symptomatic management is the main course of treatment [4]; thus, identification and exploration of mechanisms of impairment by researchers and clinicians are of significant importance.

One of the most frequent and devastating symptoms of MND is dysphagia, a group of symptoms characterised as difficulty forming the bolus and progressing it safely and efficiently from the mouth to the stomach [5]. Evidence suggests that almost all people with MND (PwMND), regardless of subtype, will eventually experience some degree of dysphagia [6]. Dysphagia in MND may occur during any stage of the swallow due to the weakening of the bulbar, respiratory and limb musculature [7, 8]. As MND progresses, individuals will experience a worsening of dysphagia symptoms, leading to complications, such as dehydration, weight loss, malnutrition and aspiration pneumonia [1, 8]. Indeed, aspiration pneumonia is the leading cause of death in this clinical population [9].

Traditionally, a compensatory approach has been taken to dysphagia management in the MND population. As part of this disease-centric reactive approach, the focus has been on palliative interventions [7]. In an effort to optimise physiological reserve for swallowing early in the disease process, there has been a recent shift towards proactive dysphagia management [10]. This approach involves proactively targeting underlying physiological function before the development of dysphagia to optimise physiological reserve. To accommodate for this shift in dysphagia management, an instrumental dysphagia evaluation which can capture discrete alterations to swallow physiology from early stages of the disease is needed to identify therapeutic targets in dysphagia treatment.

Pharyngeal high-resolution manometry (PHRM) is an emerging technology gaining increasing interest as a method for assessing pharyngeal swallow function [11]. In contrast to videofluoroscopy (VFS) and fiberoptic endoscopic evaluation of swallowing (FEES), which focus largely on swallow safety and efficiency, PHRM objectively identifies abnormalities in pharyngeal function through the quantification of pressure changes across the pharynx. To date, PHRM provides novel data on the velopharynx, mesopharynx, hypopharynx and the UES [12], all of which are affected in the MND population [1]. PHRM can clarify the biomechanical foundations of dysphagia that cannot be understood from visualisation alone, which would contribute to an enhanced, more targeted intervention plan for the PwMND. Whilst PHRM provides novel data on swallow physiology, within-subject pressure variability has been reported during volitional swallowing tasks [13]. The effect of age, pharyngeal region and volume on pharyngeal swallow pressure variability has also been established [14]. Furthermore, pressure drift has been reported across studies [15]. Each of these issues have the potential to impact markedly on clinical judgement and require further investigation before PHRM can be fully integrated into clinical practice.

Whilst PHRM would ensure the identification of subtle physiological changes of the swallow in PwMND, which, with the progressive nature of MND, could prove integral in preventing devastating dysphagia complications, there is a significant gap across the literature summarising the adoption of PHRM into dysphagia evaluation in PwMND. Such research is vital. PHRM is an invasive procedure and prevalent features of MND such as weak cough and hyperactive gag reflex could potentially impact patient acceptability and thus the overall feasibility of this assessment for PwMND [6, 7].

The primary aim of this study is to explore and summarise the use of PHRM to evaluate dysphagia in PwMND. In doing so, the following research questions will be addressed:

This study sought to explore the use of PHRM to evaluate dysphagia in PwMND. The inclusion of six publications, half of which contained a sample size of two or less participants, suggests that the current use of PHRM to evaluate dysphagia in PwMND is quite limited. This is despite the fact there has been a recent shift towards proactive dysphagia management in PwMND to optimise physiological reserve. As PHRM is being adopted into clinical practice internationally [32] the use of PHRM to evaluate dysphagia in this clinical population is likely to increase in the future.

Several important findings based on this limited data are highlighted in this review. This scoping review has demonstrated considerable variability in PHRM protocol and analysis methods in PwMND. There was variability in HRM systems used, HRM catheter dimensions, bolus volumes and consistencies administered and PHRM metrics obtained. Each of these variables can alter the pressure measurements obtained, limiting comparison of study findings [18]. Winiker et al. [31] reported considerable variability in PHRM protocol and gaps in documentation of such protocol across the literature. This review reveals that studies using PHRM in PwMND are no exception to these gaps or discrepancies. The combination of the variation in PHRM protocol and analysis methods across research centres and PHRM pressure variability with age, volitional swallow tasks and pharyngeal region previously described [13, 14] have the potential to markedly impact on clinical judgement in PHRM evaluation and warrant considerable caution until our understanding of PHRM best practice evolves. Pressure variability is of particular relevance to PwMND as this population is likely to present with impaired swallow motor control and an unpredictable swallow performance [14].

PHRM is an emerging technology and standardised guidelines for protocol and analysis methods have yet to be fully established. The PHRM international working group published the first set of protocol and metric recommendations which may streamline PHRM protocols in future dysphagia research [18]. A 5-min accommodation period, bolus delivery via syringe and the use of a solid-state HRM system with at least 10 pressure sensors 1 cm apart is advised. The magnitude of variability in the PHRM protocol and analysis methods and gaps in the documentation of such across the included studies is likely due to the fact that four out of six of the studies were published before these recommendations. One of the remaining three studies is an abstract only [28], thus justifying its lack of documentation. It is encouraging to note that full compliance to the recommendations was noted in the outstanding studies [26, 27], suggesting that the most recent publications are adhering to these preliminary guidelines. Continued compliance to the working groups’ recommendations in future publications will increase comparability of results across papers and will, in turn, enhance and further improve the understanding of the nature and course of dysphagia in PwMND.

From a PHRM feasibility perspective, PwMND across all FOIS levels in all studies that documented outcomes completed the PHRM assessment. Furthermore, the studies that reported adverse events reported that no side effects or adverse events occurred. This finding suggests that despite bulbar dysfunction in MND, PHRM is a feasible tool for this clinical population. This finding has somewhat been reflected in the previous literature. Transnasal endoscopic procedures pose similar risks to the transnasal passage of the PHRM catheter [33]. Studies documenting such procedures in PwMND have reported a high-completion rate and low incidence of adverse events [34, 35]. The advancement of the PHRM catheter through the UES, which is not seen in FEES, introduces additional considerations [33]. Whilst this is the first study to outline the feasibility of PHRM in PwMND, previous studies have documented a high-completion rate of PHRM in people with dysphagia, concluding that it is a safe and practical assessment [33]. It is of interest, however, that only one study documented patient tolerability and none of the included studies documented patient-reported outcomes of the assessment. This is a striking finding and researchers should be aware that data regarding patient tolerability are integral for an assessment that is translating into clinical practice [31]. Capturing the patients’ experience holds increased importance for this clinical population as features of MND such as hyperactive gag reflex and weak cough may impact patient acceptability significantly [6, 7]. Thus, whilst the limited data obtained suggest that PHRM is a feasible tool, gaps in documentation of patients’ experience obscures the certainty of this finding.

PHRM was used across studies to provide quantitative novel data on the velopharynx, mesopharynx, hypopharynx and the UES in PwMND. The aforementioned variability in protocol and analysis methods restricts the comparability of the metric results across the studies. Nevertheless, preliminary data published to date suggest that alterations in swallow pressure are present, and they can be identified in the velopharynx, mesopharynx and hypopharynx during swallowing. PHRM, therefore, has the potential to provide clinically useful quantitative data on swallow pathophysiology that cannot be captured through VFS or FEES. This data has the potential to inform proactive dysphagia intervention in this population to maximise physiological reserve. Of note, within-subject pressure variability has been identified across pharyngeal regions (and most notably the hypopharyngeal region) and this needs to be considered in the context of these findings [14].

When compared against normative data, the most dominant changes in swallowing physiology in PwMND highlighted through PHRM included (i) reduced pressure and contractility in the mesopharyngeal, hypopharyngeal and global pharyngeal region and (ii) evidence of UES restriction. These findings somewhat align with the previous literature as ‘changes in muscle tone’ and ‘reduced constriction’ have been previously reported [1, 7, 8]. However, this comparison further highlights that PHRM provides enhanced insight into the swallowing physiology in PwMND, as regional detail on pressure changes and exact, reliable findings of the UES have not been summarised in the literature before. Whilst these findings are based on limited data and further research is required to delineate the nature of these results, it can be concluded that PHRM offers an enhanced, comprehensive and specific insight into the changes of the swallow in PwMND.

This review highlights the potential role of PHRM to determine the discrete benefits of dysphagia interventions on swallowing in PwMND. To date, PHRM has been used in four studies to delineate specific effects of surgical and compensatory dysphagia interventions, including cricopharyngeal myotomy, sensory stimulation, increased bolus consistency and effortful swallow. The impact of cricopharyngeal myotomy on PwMND has been previously documented in a dated VFS study; reported findings were vague as the procedure was documented to ‘improve swallow function’ [36]. This review highlights that PHRM provides a much more specific and objective account of the effects of the intervention. The quantitative effects of the cricopharyngeal myotomy on the UES and velopharyngeal regions in the participant with MND were provided in the included PHRM study, rather than a descriptive subjective claim of improvement. The impact of thickened liquids has been reported to reduce pharyngeal constriction in PwMND in a VFS study [37]. These findings somewhat align with the results of the included PHRM study as reduced pharyngeal pressures were reported in response to increased bolus consistency in PwMND [25]. The PHRM study, unlike the VFS study, provided an insight into the quantitative degree of reduction, enabling a more comprehensive and definite insight into the effects of the intervention. From an effortful swallow perspective, recent research has determined that volitional swallow tasks can increase within-subject pressure variability [14]. This increased pressure variability is purported to be due to the increased task complexity and reduced automaticity of the volitional task compared to baseline swallow [14]. This issue needs to be considered when designing future PHRM study protocols. Further research into the effects of proactive dysphagia interventions on PwMND as measured by PHRM would increase clinician and researchers understanding of the nature and impact of dysphagia interventions and would ensure that only the most beneficial interventions are applied.

The findings of this review carry clinical significance as they inform clinicians of the value and viability of completing the PHRM assessment with PwMND. This review suggests that PHRM is a feasible tool for PwMND that can be utilised by clinicians to obtain a specific insight into the biomechanics of the swallow as well as an overview of the discrete and subtle effects of dysphagia interventions.

This scoping review of the adoption of PHRM into dysphagia evaluation in PwMND is the first of its kind and serves as a basis for guiding future research in this field. In order to enhance the understanding of the use of PHRM in PwMND, future research should focus on the feasibility of PHRM in this clinical population, highlighting patient acceptability and patient-reported outcomes of the assessment. Researchers should adhere to the PHRM international working groups’ recommendations and follow the protocol and select the metrics that are advised. Given the small sample sizes across all included studies, it is recommended that researchers come together and collaborate to conduct large-scaled multi-site research. This would increase the sample size, the quality of the research and in turn our understanding of the use of PHRM to evaluate dysphagia in PwMND.