This scoping review mapped and summarised the current literature describing sensory changes related to swallowing in MND, with a growing body of evidence reporting the presence of sensory changes in this population. Swallowing-related sensory function was generally described as decreased, with only a few studies (n = 4) reporting heightened sensation related to palatal and pharyngeal sensation, upper airway sensation, the cough reflex, and taste [7, 36,37,38]. Across the included studies, outcome measures assessed, and results reported were heterogeneous and characterised by poor reporting of clinically significant data.

Taste and Smell

Taste dysfunction in MND was described as ageusia of the tongue and palate, lower taste intensities, or loss in taste perception [5, 8, 44, 46, 52]. In addition, changes to olfactory perception were also reported [44, 45, 47]. Reduction of both taste and smell in plwMND may affect swallowing safety and efficiency as both have been shown to influence typical swallowing physiology. Indeed, strong flavours and olfactory stimuli are used clinically in the management of dysphagia [51, 59,60,61,62]. As such, taste and smell changes may need to be considered in the clinical assessment of swallowing in plwMND.

Beyond impacting swallowing physiology, the integration of gustatory and olfactory inputs also plays an important role in the control of appetite [63]. As such, altered processing of taste and smell stimuli may lead to reduced nutritional intake and consequently, weight loss [64]. This is important to consider as Body Mass Index (BMI) has been shown to be a predictor of life expectancy in MND [65].

An additional impact on appetite may include changes to saliva. plwMND may experience difficulty managing secretions resulting in excess saliva (sialorrhea) [66]. For example, 50% of plwMND have been estimated to experience impaired saliva production [67], with 17% reporting moderate-severe excess saliva [68], and 10% experiencing severe sialorrhea [69]. In addition, 9.1% of plwMND reported xerostomia, or dry mouth, which can result in a tenacious saliva [70]. As salivary changes may modify taste perception and hence influence appetite and eating-related pleasure, saliva status, taste and appetite should all be considered during swallowing-related assessment in plwMND.

Cough Reflex and Gag Reflex

Sensory function is not only critical for the initiation, execution and modulation of swallowing-related biomechanics, but also contributes to airway protection mechanisms. As part of these mechanisms, the cough reflex plays a vital role in expelling foreign material from the airway, consequently limiting aspiration and reducing risk for aspiration pneumonia [37]. Similarly, the gag reflex can prevent substances from prematurely entering the pharynx, larynx, or trachea [71]. Growing evidence has highlighted the reduction or absence of gag and cough reflexes in MND [7, 10, 39, 54]. In the context of reports that document the presence of silent aspiration [8, 10, 55] in plwMND, cough reflex testing should be considered in swallowing examination in MND. Future studies may also benefit from investigation into the differences in cough reflex across MND phenotypes related to the presence or absence of upper motor neuron involvement and hyperreflexia. At present, this analysis is unable to be completed due to the unspecific and heterogeneous language used to describe MND phenotypes in the included literature.

Impaired tactile sensation in the larynx [4, 6, 8, 42], pharynx [36], and upper airway [54] may also contribute to the prevalence of impaired cough reflex [10, 37, 54] and gag reflex [39] in this population. Despite the presence or absence of a gag reflex not being an indicator of dysphagia [71], this information further lends to the necessity for sensory investigation of structures involved in swallowing during swallowing examinations in MND, with continued monitoring throughout the disease process to ensure swallow safety.

Somatosensory Function

Bolus properties have been shown to impact a variety of swallowing metrics, including upper oesophageal sphincter (UES) opening duration and opening extent, pharyngeal peak pressure, and hypopharyngeal intrabolus pressure [72]. The included literature describes a range of changes to tactile sensation in plwMND including reduced sensitivity to tactile stimuli in the larynx [4, 6, 8, 42], palate and pharynx [36], and tongue [41]. Reduced sensitivity in these areas may impact detection of somatosensory information relating to the properties of a bolus, including its size, consistency, temperature, weight, and velocity, which heavily influences swallowing physiology across all phases of swallowing [73, 74]. These bolus properties have been shown to impact a variety of swallowing biomechanical metrics, including UES opening duration and opening extent, pharyngeal peak pressure, and hypopharyngeal intrabolus pressure [72].

Further, the use of analgesics for pain management in plwMND may pose an additional cause for changes to somatosensory function and subsequent changes to swallowing biomechanics. Analgesics that inhibit the somatosensory system, including changes to perception of temperature, are suggested for use in plwMND to manage muscle pain [75,76,77], and have been linked to increased aspiration risk [78]. Thus, review of current medications and their potential impact to swallow biomechanics should be considered when assessing and managing dysphagic plwMND.

Implications for Swallow Safety

This review revealed a growing body of literature reporting changes to smell, taste, the cough and gag reflexes, and somatosensory function in plwMND, all of which are relevant for safe and efficient swallowing. Beyond their impacts on swallowing biomechanics, changes to these sensory functions are likely to contribute, at least in part, to reports of absent laryngeal adductor reflex [6], or the high incidence of silent aspiration in this population [8, 10, 55].

It is, therefore, important to consider how sensory changes may interact with swallowing function, especially in the context of likely impairment of swallowing-related motor function in MND. For example, in non-impaired motor systems, increased motor output may compensate for changes in sensory function [79,80,81,82,83,84,85,86,87,88,89,90]. Reduced motor function in MND may limit such compensatory mechanisms for sensory changes in addition to the decline in swallowing motor function driven by degeneration of the motor system. As such, swallowing safety and efficiency in plwMND may be at risk from both sensory and motor changes, which need to be considered in swallowing assessment and management.

Interaction of sensory changes reported in MND with natural ageing process.

It is important to recognise that the changes in sensory function in MND collated in this review may, at least in part, also be related to the natural ageing process. With the average age of onset of MND being 58 years [91], natural sensory decline as the result of advancing age poses a potential alternative cause for the sensory loss described in plwMND. The natural aging process is associated with a range of impacts on sensations relating to swallowing, including taste [79, 81,82,83, 88, 89, 92], smell [80, 85, 87, 90], and the cough reflex [84, 86], all of which have been implicated in plwMND. It should be noted, however, that while sensory changes have been reported as part of the natural ageing process, these changes are more likely to occur at an older age than the average age of onset of MND (58 years). In addition, plwMND have been reported to experience sensory changes that are not typically described in the literature as occurring within the natural ageing process, including changes to tactile sensation of the palate, pharynx, larynx, upper airway, and tongue. Therefore, on balance, we propose that the changes to sensory function summarized here are more likely to be related to MND-specific disease processes than ageing.

A Comment on Changes in Sensory Function in Frontotemporal Dementia (FTD) and Facial Onset Sensory and Motor Neuronopathy (FOSMN)

A pertinent theme established in the included literature was that of MND being a “multisystem disorder”, implicating systems other than only the motor system. One such example of this is found in the growing links between MND and frontotemporal dementia (FTD) [93, 94]. It is estimated that 15% of plwMND will develop a frank FTD [94]. People living with FTD have been observed to experience impaired olfaction [95,96,97], similar to that described in the included literature pertaining to plwMND. This highlights a key clinical consideration for sensory testing in dysphagic plwMND, particularly when FTD is present or suspected.

An additional consideration relates to the emerging literature discussing a disease that features sensory disturbance with potential links to MND – facial onset sensory and motor neuronopathy (FOSMN) [98,99,100]. While the etiological and pathophysiological mechanisms underpinning FOSMN remain unclear, it poses a potential phenotype of MND of which sensory dysfunction appears to be a hallmark feature. Similar to MND, dysphagia is frequently reported in people living with FOSMN [99, 101,102,103]. Taste disturbance, absent gag reflex, and absent palatal and pharyngeal reflexes have also been reported in this population [98, 99, 101, 102].

Exploration of the roles of FTD and emerging MND phenotypes in the presence of sensory disturbance in plwMND was not the focus of this study. However, specific evaluations of these conditions require further research.

Limitations

This review included only articles in English. We acknowledge that this may result in relevant literature that was published in a different language being excluded. The included literature in this scoping review is characterized by heterogeneity in its outcome measures and methods, impacting our ability to establish patterns of sensory change in plwMND. Furthermore, many studies included data that was not objectively assessed, with no baseline measurements available, resulting in low research reliability. Demographic and clinically significant information, such as disease severity and onset, dysphagia severity and onset, and consistency of food and liquid trials, were frequently not discussed in the included literature. This worked to further compound the difficulty in drawing clinical conclusions from the literature.

Additionally, very few studies took multiple measurements or replicated their results. As such, data reported in the included literature are likely to have low validity due to unknown levels of variability as well as low reliability. It is acknowledged that the reason for single measurements likely relates to (i) limited resources, (ii) accelerated disease degeneration impacting ability to complete multiple assessments, and (iii) limited life expectancy.

Due to the heterogeneity in study designs and outcome measures reported, we were unable to describe universally applicable patterns of sensory change in MND. However, here we suggest key areas to consider within both clinical practice and future research.

Clinical Practice and Research Implications

While the current clinical guidelines for MND management make reference to the importance of swallowing assessment and management, they do not discuss how sensation should be considered in this process [76, 104]. Based on the findings of this review, we propose that the assessment and management of swallowing function in plwMND should, as individually appropriate, consider changes to olfactory, gustatory, and somatosensory function related to swallowing. Further, the impact of these changes on swallowing safety mechanisms, along with psychosocial implications, should continue to be monitored throughout disease progression.

Overall, this review highlights limited and contradictory knowledge regarding sensory changes related to swallowing in MND. The generally low quality of evidence in this area is a call to arms for thorough, high-quality investigations into sensory changes in MND. Research using control groups, longitudinal testing, and consistent evidence-based outcome measures is required to confirm the presence of sensory deficits related to swallowing in plwMND. Replicating existing studies with the same outcome measures may improve validity and reliability of the data. In addition, the included literature subjectively describes the degree of sensory change present, often in comparison to healthy cohorts. Studies have not yet, however, taken steps to accurately describe the effect size. This limits our ability to estimate the presence and magnitude of sensory changes in plwMND. Finally, we suggest that investigations into how sensory deficits are contributing to, and interact with, dysphagia in plwMND are also warranted.