Impaired foot vibration sensitivity is related to altered plantar pressures during walking in people with multiple sclerosis

Balance and walking impairments have been reported by approximately 90% of those with multiple sclerosis (MS), with a majority indicating a “moderate” or “high” impact on quality of life (Hemmett et al., 2004). Although the etiology of these impairments is likely multifactorial (Van Emmerik et al., 2014) and varies among individuals, including elements of symptomatic fatigue (Coote et al., 2013), spasticity (Nilsagard et al., 2009), strength (Chung et al., 2008) and central motor drive (Miehm et al., 2020; Ng et al., 2004), reduced mechanoreception may play a significant role. Individuals with MS demonstrate diminished cutaneous sensation (vibration sensation, two-point discrimination, light pressure sensation) of the foot's plantar surface that worsens in progressive vs. relapsing-remitting forms, as well as in fallers vs. non-fallers (Citaker et al., 2011; Jamali et al., 2017; Kelleher et al., 2010; Miehm et al., 2020; Peebles et al., 2018; Soyuer et al., 2006; Van Emmerik et al., 2010). Individuals with MS who exhibit diminished plantar sensitivity also demonstrate performance decrements on balance tests—including decreases on timed tests (Citaker et al., 2011), and increased center of pressure (Porosinska et al., 2010; Van Emmerik et al., 2010) or trunk sway (Corporaal et al., 2013; Findling et al., 2011) during quiet standing and dynamic tasks (Van Emmerik et al., 2010); similar decrements are evident among those with MS when sensory conditions are manipulated (Cattaneo and Jonsdottir, 2009; Fjeldstad et al., 2009; Porosinska et al., 2010; Spain et al., 2012). Certainly, reduced cutaneous sensation impacts standing balance in this population (Van Emmerik et al., 2014), however the relationship between reduced plantar sensation and walking among those with MS is less well established. Individuals with MS demonstrate gait alterations (Benedetti et al., 1999; Comber et al., 2017; Gianfrancesco et al., 2011; Huisinga et al., 2013; Kaipust et al., 2012; Kalron et al., 2013; Kelleher et al., 2010; Martin et al., 2006; Remelius et al., 2012; Socie et al., 2013; Sosnoff et al., 2012; Spain et al., 2012), which likely indicate impaired walking balance. Despite growing evidence of the negative impact of sensory impairment on balance in people with MS, few gait studies have also assessed plantar sensation; those that did demonstrated altered gait mechanics associated with impaired plantar sensation (Kelleher et al., 2009; Remelius et al., 2012). However, further study into how reduced plantar sensation may modulate gait alterations in MS is needed.

One means of probing this relationship is to evaluate the foot's plantar surface for insensate regions, and relate this to the distribution of plantar pressures during walking. Plantar pressure distributions during walking generally proceed from the lateral heel at foot contact, transit through the midfoot at midstance, then move medially as push-off is initiated, finally moving towards the 5th phalanx at toe-off. These patterns are affected when walking speed (Segal et al., 2004) or footwear (Franklin et al., 2015) are manipulated, with increased pressure as speed increases, and at the heel and metatarsals when barefoot (Carl and Barrett, 2008), although habitual barefoot walkers demonstrated pressures that were more evenly spread across the foot (D'AoÛt et al., 2009). Plantar sensation does seem to impact plantar pressures, although equivocal results have been demonstrated under experimental and pathological conditions. Anaesthesia targeting plantar mechanoreceptors demonstrated no impact on plantar pressures (Höhne et al., 2009), while reduced plantar sensation through ice immersion was associated with a forward and lateral shift toward the metatarsals (Taylor et al., 2004), decreased plantar pressures and a cautious, flat-footed gait pattern (Eils et al., 2002). Adults with diabetic neuropathy, who often have significant mechanoreceptive and proprioceptive impairments, demonstrate altered pressure distributions during quiet standing (Zhang and Li, 2013) and a pressure shift towards the forefoot during walking (Savelberg et al., 2009). An inverse relationship between sensory thresholds and plantar pressures has even been demonstrated among young, healthy adults (Nurse and Nigg, 1999), suggesting a fundamental link between plantar sensation and foot pressure.

Among those with MS, impaired plantar sensation has been reported (Citaker et al., 2011; Kelleher et al., 2009); although less profound than those with neuropathy, reduced sensation may exert a significant impact given the balance impairments typically demonstrated in people with MS. Although two studies (Abdurakhmanov et al., 2006; Keklicek et al., 2018) evaluated pressure patterns among those with MS, neither attempted to relate these patterns to plantar sensation, nor did they control for or report walking speed. Given the impact of walking speed on plantar pressures, it is vital that speed is controlled if between group comparisons are to be made. We propose that in order to probe whether impaired plantar sensation and plantar pressures are linked during walking, a full characterization of regional sensory thresholds and plantar pressures across a range of gait speeds must be undertaken.

Therefore, the purpose of this study was to determine the relationships between plantar vibration sensation and pressures during walking. We examined: (1) whether individuals with MS who demonstrate reduced plantar vibration sensation (i.e., heightened vibration perception thresholds) also demonstrate altered plantar pressures when compared to an age- and sex-matched control cohort; (2) how these relationships change between more and less affected sides; and (3) how these relationships change with walking speed.

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