Diagnosis of Swallowing Disorders: How We Interpret Pharyngeal Manometry

Characterising UES relaxation and opening is important for the assessment of swallowing disorders. UES relaxation/opening failure can occur due to structural pathology, problems with integrative neuro-sensory function and/or failure of neuro-muscular mechanisms. Relaxation and opening of the UES is a complex process, modulated via sensory inputs, changing the duration of relaxation and the extent of opening in relation to the bolus swallowed. Larger boluses travel at a faster flow rate through the pharyngo-esophageal segment, and normal swallowing allows this to occur without substantially increasing the flow resistance [1•, 2•, 3‐5]. Hence, by changing the volume and consistency of the boluses swallowed, it may be possible to reveal structural pathology or sensory misregulation of swallowing.

At rest the UES can be identified by the presence of a high pressure zone generated by cricopharyngeus (CP) muscle contraction. During swallowing, the CP muscle deactivates, remains inactive whilst the UES lumen opens then closes, then the CP re-activates. The suprahyoid muscles, mechanically coupled to the UES, and the distension forces generated during bolus passage govern luminal opening/closure during CP inactivity. Whilst manometry alone cannot easily elucidate UES opening and closure, radiology, or its non-radiological surrogate, intraluminal impedance denoting bolus presence and flow, can [2•].

We routinely assess UES tonic contractility using pre-deglutitive basal pressure (UES-BP, Fig. 1b) and extent of UES relaxation using the UES integrated relaxation pressure (UES-IRP, Fig. 1b) [16••, 25, 26•]. At this time, there are limited published data available from patients with UES obstruction. However, UES IRP values have been shown to increase with age [16••, 26•] and are elevated in subjects with motor neurone disease [16••], but interestingly not consistently in subjects with radiological cricopharyngeal bars [16••], showing that this pathology is not always obstructive in nature.

We use impedancometric measurements to determine information on pharyngeal and UES opening. The nadir impedance value [17] during bolus swallowing, or its inverse, maximum admittance (used henceforth), can be used to infer the maximum extent of luminal opening during bolus flow. When measured within the UES region, the maximum UES admittance (Max UES Adm, Fig. 1c) is reduced in dysphagic patients and therefore appears to be an excellent non-specific measure for UES dysfunction [16••].

The hypo-pharyngeal maximum admittance, corresponding to maximum distension of the hypopharynx, objectively defines a time point for determining intra-bolus pressure during maximum bolus distension (IBP, Fig. 1e). IBP is the mechanical consequence of lingual and pharyngeal propulsive forces and the diameter of the lumen. Per volume swallowed, an abnormally high IBP can be a marker of flow restriction due to structural pathology [18•, 19, 20] or, alternatively, a high IBP can be a marker of sensory misregulation of the swallow leading to failure to accommodate for bolus size and the bolus transiting the pharyngeal chamber more rapidly [21•].

An important caveat when using IBP diagnostically is that IBP can only discriminate a pathological UES restriction of bolus flow when the pharynx has sufficient contractility to both propel the swallowed bolus distally and seal the lumen proximal of the bolus domain, preventing retrograde bolus escape [9, 19]. We use mean hypo-pharyngeal peak pressure (PeakP, Fig. 1e) and UES peak pressure (UES PeakP, Fig. 1b) to define the strength of contractility. These pressures are influenced by several factors. The strength and sequencing of neural activation and muscle fibre density of the swallowing muscles are most important. However, other passive factors, such as luminal diameter and pharyngeal wall thickness, are also important as they determine the degree of muscle shortening required in order to bring the lumen to a point of closure (i.e. influencing the length-tension properties of the swallowing muscles). Pharyngeal pressures are reduced in neuromuscular diseases such as motor neuron disease [16••] and other diseases affecting the musculature directly such as myopathies or myositis [20]. Interestingly, subjects with cricopharyngeal bars [16••] also have reduced pharyngeal pressures, implying this phenomenon may be a manifestation of pharyngeal neuromyopathy. Overall, abnormalities of pharyngeal contraction are rare and weakness should prompt a determined search for an underlying neuromuscular pathology. It is also important to keep in mind the important function of suprahyoid muscles in opening the UES, so that a reduction in UES opening (seen as a low UES Max Adm) can occur in concert with pharyngeal weakness, because of muscle weakness more globally.

Finally, in addition to guiding IBP measurement, the admittance profile of the hypopharynx provides an estimate of the bolus presence time (BPT, Fig. 1d) and the latency period from distension (maximum admittance) to contraction (DCL, Fig. 1e). Mistiming of swallow coordination is likewise an important determinant of pre-swallow aspiration [22•]. A short BPT or DCL could indicate perturbation of sensory afferent mechanisms leading to an inability to modulate the swallow to accommodate different volumes. Poor-oral bolus containment (failure of lingual propulsion) results in a short DCL (because the major forces driving propulsion switch from predominantly lingual to being predominantly pharyngeal; refer to descriptions of the phases of bolus flow in the “Qualitative Assessment of Swallow Recordings” section below). Whilst a long BPT may suggest pre-swallow bolus presence and/or post-swallow residue [22•].

We use two measures to determine global pharyngo-esophageal swallowing dysfunction; namely the swallow risk index (SRI) to estimate aspiration risk [23••] and post-swallow impedance ratio (PSIR) to estimate post-swallow residue [24••]. The SRI (Fig. 2) formula [23••] combines four hypo-pharyngeal measures to derive a single value representative of global swallowing dysfunction and aspiration risk. Post-swallow residue is an important determinant of aspiration on subsequent swallowing [7•]. Impedance values are lower (admittance higher) when the pharyngeal chamber contains bolus residual [24••, 27]. The PSIR relates impedance during swallowing to the impedance after pharyngeal contraction to derive a single value correlating the degree of post-swallow residual [24••] (Fig. 1f).

As pharyngeal swallowing and UES relaxation occurs rapidly, it can be challenging to assess the recordings without image manipulation. We find it most helpful to magnify the recording so that a 3–5-s interval fills the entire screen

As shown in Fig. 3a, each swallow can be qualitatively assessed for weak pressures at the velopharynx and tongue base, hypopharynx (including discreet gaps in the pressure sequence) and at the UES. UES relaxation and mistiming of flow events can also be assessed. Specific note should be taken of simultaneous “pan-pharyngeal” intra-bolus pressurizations, which are never seen in health and indicative of distal obstruction in combination with non-lumen occlusive pharyngeal contraction.

Qualitative information is also contained in the admittance and pressure curves in the hypopharynx and at the UES. The hypo-pharyngeal admittance during pharyngeal deglutition can often show separate phases of bolus flow. As originally described by Pal et al. [8], there are two phases of bolus motion during normal swallowing (Fig. 3b). Phase 1 is dominated by tongue-induced bolus acceleration (lingual propulsion). In normal circumstances, UES opening occurs as the bolus encounters the UES producing little of no resistance to bolus flow during phase 1. During phase 2, the bolus is driven through the open UES at a constant speed by the pharyngeal stripping wave (pharyngeal propulsion). The hypo-pharyngeal admittance waveform is indicative of this bolus motion (Fig. 3c). In health, the waveform usually appears as a single peak, with the initial rise of admittance from baseline corresponding to when lingually propelled bolus enters the hypopharynx (closure of velopharynx can also be seen to occur at this point) and the admittance peak corresponding to maximum luminal distension. A single peak suggests that lingual and pharyngeal propulsion phases are coalescent. Appearance of a double peak, meaning that the phases are separately discernible from each other, may suggest either the following: (i) phase miss-timing (e.g. phase 1 precedes UES opening) and/or (ii) that the rate of flow during one of the phases is being disproportionately slowed (e.g. flow resistance during phase 2).

We have provided some more information and examples of the above commentary in the “Example Patient Cases” section below.

Qualitative assessment (Fig. 4) suggests that pressure generation is intact. Hypo-pharyngeal admittance shows some evidence of pre-swallow bolus presence and separation of the lingual and pharyngeal phases of propulsion. Hypo-pharyngeal distension pressures are low during lingual propulsion (phase 1) but increase during pharyngeal propulsion (phase 2). UES pressures show complete UES relaxation. The pattern of distension pressure increase, which is absent during lingual propulsion and emerges during pharyngeal propulsion, is evidence for luminal restriction inferior to the UES.

Quantitative assessment (Fig. 9) showed that all swallow function variables were within normal limits. These findings are in keeping with radiology, which showed occasional premature spillage to the hypopharynx, no aspiration (penetration-aspiration scale (PAS) = 2; Material enters the airway, remains above the vocal folds, and is ejected from the airway) and only minor levels of post-swallow residue. The measured degree of flow resistance was low (normal IBP) suggesting only minor obstructive pathology. Radiology showed no-obvious stricture. However, as the pattern of intra-bolus pressurisation described above cannot be considered normal (i.e. not seen in healthy subjects), this situation should be monitored and a repeat investigation performed should symptoms worsen.

Qualitative assessment (Fig. 5) suggests that pressure generation was globally weak, with a notable absence of hypo-pharyngeal constrictor activity and no visible hypo-pharyngeal distension pressures. Hypo-pharyngeal admittance shows no evidence of pre-swallow bolus presence. There is no separation into the lingual and pharyngeal phases of propulsion. However, in this patient with weak/absent pharyngeal activity, the single admittance peak most likely represents lingual propulsion only.

Quantitative assessment (Fig. 9) showed an abnormal SRI, consistent with aspiration risk, and abnormal PSIR, consistent with significant post-swallow residual. These global findings are in keeping with radiology, which shows significant post-swallow residue in both the valleculae and piriform sinuses, leading to post-swallow aspiration (PAS 5; Material enters the airway, contacts the vocal folds, and is not ejected from the airway).

The specific pressure variables confirmed profound weakness of the hypo-pharyngeal constrictor’s and criocopharyngeus muscle activity. Both pre- and post-deglutitive UES contractility were abnormal. Measures of intra-bolus pressure, UES opening and flow timing were all normal, consistent with good lingual bolus propulsion and sufficient UES opening. Note: In circumstances of absent, “non-propulsive”, hypo-pharyngeal contractility, low IBP reading do not necessarily exclude reduced UES opening and the literature suggests that cases of inflammatory myopathy are often associated restricted sphincter opening [20]. However normal UES admittance values confirm that UES opening is adequate in this case. These findings suggest that lingual and suprahyoid muscle function are less involved at this time (moderate pressure generation can be seen at the tongue base on the qualitative assessment).

Qualitative assessment (Fig. 6) suggests that pressure generation is intact. Hypo-pharyngeal admittance shows no evidence of pre-swallow bolus presence. There is no clear separation of the lingual and pharyngeal phases of propulsion and hypo-pharyngeal distension pressures increase immediately with the onset of lingual propulsion suggesting flow resistance at the level of the UES (in contrast to case 1, who exhibits evidence of flow resistance below the level UES). UES pressures show incomplete UES relaxation.

Quantitative assessment (Fig. 9) showed an abnormal SRI, consistent with aspiration risk, and abnormal PSIR and BPT, consistent with significant post-swallow residual. UES maximum admittance was abnormal consistent with restricted UES opening. Of specific swallow function variables, findings of a high IRP, high IBP and short DCL are consistent with abnormal flow resistance at the UES. Contractility of the hypopharynx and UES was normal. These findings are in keeping with radiology showing obstructive pathology. Most notably an impression occluding >50% of the lumen at the level of UES. Prominent cervical osteophytes were also noted below the level of UES. The penetration-aspiration scale on radiology revealed laryngeal penetration (PAS = 5; Material enters the airway, contacts the vocal folds, and is not ejected from the airway).

Qualitative assessment (Fig. 7) suggests that pre-deglutitive UES basal pressures were disproportionately lower than UES contractile pressures. Hypo-pharyngeal admittance shows bolus presence prior to UES opening. There is clear separation of the lingual and pharyngeal phases of propulsion. However, in contrast to case 1, phase 1 is mistimed and precedes UES opening. Hypo-pharyngeal distension pressures indicate flow resistance at the level of the UES.

Quantitative assessment (Fig. 9) showed an abnormal SRI, consistent with aspiration risk, and abnormal PSIR and BPT, consistent with significant post-swallow residual. UES maximum admittance was abnormal, consistent with restricted UES opening. Of specific swallow function variables, findings of a high IRP, high IBP and short DCL are consistent with abnormal flow resistance at the UES. Pre-deglutitive UES basal tone was weak in contrast to contractility of the hypopharynx and UES which were normal.

These findings are consistent with UES dysfunction due to combined neuro-myogenic and structural changes, namely neural de-innervation leading to weak contractility and muscle inactivity in turn leading to loss of muscle compliance. Suprahyoid muscle involvement results in failure of the extrinsic UES opening mechanism. Consequently, the UES must be pushed open by the intra-bolus pressure generated by luminal closure of the pharyngeal chamber above. CP muscle involvement results in low tone and loss of compliance meaning that the pharynx must work even harder to achieve trans-sphinteric flow. Marked decompensation of the swallow can be anticipated if pharyngeal contractility, currently least affected, weakens as a consequence of MND progression.

Radiology revealed difficulty with oral bolus control, with subsequent premature bolus spillage. There was significant pharyngeal residue, when swallowing bolus of increased consistency. Cricopharyngeal bar inferior to the UES was evident; however, its location suggests that it is not obstructive to bolus flow. There was some evidence of laryngeal penetration during liquid swallows (PAS = 3; Material enters the airway, remains above the vocal folds) and marked residue retention during semi-solids.

Qualitative assessment (Fig. 8) shows a highly abnormal swallow. Hypo-pharyngeal admittance shows bolus arriving within the pharynx well ahead of any attempt to swallow. The pharynx remains dilated with bolus for the duration of this tracing. An attempt to swallow causes pan-pressurisation of the pharyngeal chamber. However, the hypo-pharyngeal admittance remains elevated indicating that the lumen does not close. The UES does not relax during the attempt swallow, consistent with a persistent, neurogenically driven muscle tone (as previously described in neurogenic dysphagia [9]), and UES admittance does not increase, consistent with UES not opening and the pharyngeal chamber failing to empty.

Quantitative assessment (Fig. 9) showed an extreme SRI, consistent with aspiration risk, and abnormal PSIR and BPT, consistent with significant post-swallow residual. UES maximum admittance was abnormal, consistent with reduced UES opening. Every swallow function variable, with the exception of pre-deglutitive UES basal tone, was highly abnormal in this case.

These findings are consistent with total failure of pharyngeal swallow.

These findings are in keeping with radiology showing premature spillage of the bolus due to poor oro-lingual control, non-opening of the UES, with consequent retention of bolus in the hypopharynx and overt aspiration (PAS = 8; Material enters the airway, passes below the vocal folds, and no effort is made to eject).

The patient had a major ischemic brainstem stroke affecting several aspects of his oropharyngeal swallow. Despite mechanical dilatation and botulinum toxin injection of the UES, he remains dysphagic after 6 months related to incoordination of the swallow response and profound pharyngeal weakness. The extreme level SRI reinforces the catastrophic, multi-factorial, nature of the disorder and therefore likely failure of therapies that target the UES only.