Multiple sclerosis (MS) is a chronic autoimmune inflammatory disease of the central nervous system characterized by a demyelination of the white matter with damage to the axons. It progresses in spurs and mostly affects young adults (i.e., aged between 20 and 40). As there is no causal treatment of MS, therapies used prevent or minimize symptoms. The MS symptoms (Jakimovski et al., 2024) differ according to individuals (Ghorbanpour et al., 2023), but the most common are muscle weakness, muscle hyperactivity or spasticity; sensory symptoms (paraesthesia); visual symptoms; sphincter, sexual, cognitive, and psychiatric disorders; severe fatigue; pain; and walking disorders (Ghorbanpour et al., 2023; Jakimovski et al., 2024). A thorough assessment of gait is essential, since among the symptoms mentioned above, people with MS (PwMS) report that walking is the most affected function and that it should be treated as a priority (Ghorbanpour et al., 2023). Commonly, walking disorders can be treated with physiotherapy (Etoom et al., 2018) or drug-based medication (Goodman et al., 2015). Although drugs have little role to play in this disability (Surya, 2015).

To determine the best treatment to improve PwMS’s walking performance; several assessments are conducted to evaluate the level of walking impairment. The most common is the expanded disability status scale (EDSS) (Cohen et al., 2023; Naseri et al., 2021). The EDSS is rated from 0 to 10, and scores between 4 and 7.5 related exclusively to PwMS’s walking distance and the needs of technical aids for walking (Meyer-Moock et al., 2014). To classify PwMS, EDSS does not provide additional information on walking pattern or the ability to perform other daily living activities which depend on walking capacity. Additional walking tests are frequently administered alongside EDSS to reinforce its assessment (Bethoux and Bennett, 2011; Skjerbæk et al., 2019).

Several studies have focused on quantified walking analyses of PwMS. In terms of spatial-temporal walking parameters, it is well documented that when compared with healthy controls, PwMS have reduced walking velocity, cadence, swing phase and stride lengths and an augmented double support phase (Comber et al., 2017; Kelleher et al., 2010; Severini et al., 2017). These variations reflect a deteriorated walking pattern which is caused by neuromuscular dysfunction. A reduction in hip, knee and ankle range of motion (ROM) has been observed during walking (Filli et al., 2018; Kelleher et al., 2010; Severini et al., 2017). These results suggest the importance of knowing upfront the state of PwMS’ joint function: whether PwMS’s have adequate ROM, strength, and absence of spasticity. These analytical assessments are often conducted by a physiotherapist when a neuro-orthopaedic check-up (NOChU) is performed (Decavel and Sagawa, 2019).

The limited research on NOChU for PwMS shows that loss in ROM, although not originally a primary problem, can become one, particularly due to spasticity and motor control disturbed (Benedetti et al., 1999; Haselkorn and Loomis, 2005; Hoang et al., 2014). Joint stiffening becomes a first body response to the problem of postural control in walking (Benedetti et al., 1999), as, although it limits velocity and stride length, it improves the patient’s balance and stability. However, in the long term, there is a negative impact on the maintenance of the musculoskeletal system, leading to difficulty in people’s daily living activities and independency (Hoang et al., 2014; McNicholas et al., 2018). Moreover, this phenomenon is observed even in PwMS at the early stages of the illness (Benedetti et al., 1999).

While walking appears to be assessed by different approaches (e.g., EDSS, quantified walking analysis), few studies have focused on the NOChU and even less on the simultaneous analyses of walking disorders and the NOChU for a same PwMS sample. Thus, the intention of study was therefore to determine the association of the potential deficits identified during the NOChU that comprise tests of ROM, strength, and spasticity on walking functions of PwMS. This study aims to provide a better understanding of the effect of joint and muscle deficits on walking, and them, contribute to decision-making in physiotherapy.

A retrospective search in the laboratory database, including NOChU and walking assessments that were conducted for the period of 5 years. The study was approved by the ethics committee of the University Hospital of Besançon (No. 13/405) and the French Health Products Safety Agency (No. 2013-A002305-56). All patients in the study gave their written and informed consent.

The total number of patients evaluated over a 5-year period in the laboratory was 212. However, 107 patients were excluded from the study due to lack of data, whether regarding NOChU and/or walking assessment. Since these data must be collected at the same time. Therefore, Table 1 shows the characteristics of 105 PwMS who met all inclusion/exclusion criteria. Sixteen patients were included in the light group, 49 in the moderate group, and 40 in the high group. Their mean±SD age, height, weight, and BMI amounted to 51±12 years of age, 1.67±0.10 m, 75±15 kg, and 27±5 kg/m² (i.e., overweight according to the World Health Organization classification), respectively. The median (IQR) EDSS level was 4.5 (6–4).

Although NOChU and walking evaluations are often practiced in PwMS clinical routine (Hoang et al., 2014; Mañago et al., 2018; Picelli et al., 2017), few studies are dedicated to NOChU and associate these two evaluations in a same population. This could bring new insights to determine the role of each joint and muscle during a routine physiotherapy assessment in a functional activity such as walking and then improve decision-making for therapeutic strategy. Initially, aspects related to NOChU (ROM, muscle strength, and spasticity) will be discussed, followed by walking assessment, and finally we will comment on the interactions between them. Regarding aspects relating to ROM, the hip mobility is relatively preserved except at extension. This deficit could be disturbing in daily living activities and leads to walking disturbances such as a diminished posterior step length. PwMS in the high group had a hip extension of 20°, which is considered as the minimum physiological extension necessary for walking at comfortable velocity (Hermez et al., 2023). This result suggests that more demanding walking conditions such as negotiating obstacles, increase walking speed or walking on an uneven ground could be challenging for PwMS. The knee extension was also limited with a mean value close to 0°, against a normal physiological value of a recurvatum of 10° (Kapandji, 2011). Despite this theoretical limitation, during walking and other daily living activities (Fig. 1B), the amplitude required does not exceed 0° suggesting that these limitations have a small impact on these activities.

Compared to all joints studied, the ankle was the most impaired, especially for the dorsiflexion. These results corroborate the only study that analysed a similar population sample (Hoang et al., 2014). The high group has a mean ROM of 17°. This value is very close to the walking limit at comfortable velocity, and remains below the value required to perform other activities. The physiological ROM for climbing and descending stairs is 20° (Hermez et al., 2023). This implies that PwMS must compensate with strategies such as hip-hinking, circumduction, vaulting or steppage to accomplish these daily tasks (Hermez et al., 2023). This limitation of the dorsiflexion is even more obvious when the knee is fully extended with a mean of 10°. These results suggest a hypo-extensibility of triceps sural (Krause et al., 2011). In an equivalent scenario, during the walking at the end of the double support phase, the knee is fully extended, and the ankle should be at 15°. In this walking phase reduced ankle dorsiflexion can have a negative impact on toe clearance preventing the passage for the next step, and consequently cause loss of balance, falls, or slower speed gait. Collectively for a physiotherapy strategy, it seems important to maintain ROM before it deteriorates throughout the MS course or to improve it if a ROM limitation already exists (Hoang et al., 2014). As it was previously observed and, in this study, in general, the above-mentioned loss of ROM is not a primary problem in PwMS, although it may eventually lead to joint retraction (Haselkorn and Loomis, 2005). Other factors that may affect joint retraction are strength and spasticity (Hoang et al., 2014).

Considering muscle strength, PwMSs were divided into two categories: <3 or ≥3 MRC scale. For walking, individuals need more than the equivalent to the force against gravity because of the extra load bearing joints (i.e., weight of the trunk (Sagawa et al., 2017), head, limbs...). The movement is no longer analytical and concentric as done during NOChU, but is a functional complex movement with concentric, isometric, and eccentric contractions (Fang et al., 2004; Hughes et al., 1996). Despite the different methodological approaches previous studies (Hoang et al., 2014; Mañago et al., 2018) showed a decline of strength in relation to the severity of MS. The loss of strength seems to be more important than those observed in our study (Hoang et al., 2014; Mañago et al., 2018). Although they used handheld dynamometry, not manual tests. Even if the weakness impairs walking (Hameau et al., 2017), our results suggest that muscle strength does not appear to be problematic for the majority of PwMS. In fact, for the hip and ankle, about one-fifth of PwMS had strength of 3 or less, and about one-quarter of PwMS had the same knee strength. The most deficient muscle group was the knee flexors; for about a third of PwMS. Another aspect of strength that was not measured in this study, is muscle fatigability. As walking is a cyclical movement, its observed degradation (Table 6) could be better associated with the capacity of a joint exercise repetition (Hameau et al., 2017). However, further studies are needed to confirm this hypothesis. In relation to spasticity, PwMS were divided in two groups according to the presence of a catch angle. A catch angle might induce discomfort while walking (Norbye et al., 2020). At hip level, there were few PwMS with spasticity greater than or equal to 2. However, for these patients the catch angle for hip flexors was at 27°. Indeed, this can have an impact on walking at the beginning of the support phase when the lower limb is moving towards hip extension (Fig. 1) (Norbye et al., 2020). At knee level, there were few patients with spasticity greater than or equal to 2. However, for them, the catch angles for the flexors and extensors were 85° and 71°, respectively. During the walking, the catch angle of the extensors could cause discomfort at the beginning of the swing phase when they must flex the knee (Hermez et al., 2023). The catch angle of the flexors could also cause discomfort at the end of the swing phase when they must extend the knee and supported the foot on the ground to start a new gait cycle. However, during the stance phase, there is a minimal impact of these catches as the joint ROM required during this phase is lower (about 20°) than the observed catch angles (Hermez et al., 2023).

The most affected joint was the ankle, particularly the sural triceps and soleus (52% and 62% of PwMS had spasticity greater than or equal to 2, respectively). This result corroborates a previous study (Norbye et al., 2020). This spasticity is present during dorsiflexion. Moreover, the ankle was also concerned by the most affected passive ROM (Table 2). The catch angle for the posterior leg muscles is on mean −2°. This angle may affect daily living activities, starting with walking. This angle could interfere in the swing phase when the ankle must dorsiflex; this could cause falls as the toes drag. The catch angle could also interfere during the stance phase when the tibia must move forwards in relation to the foot (Hermez et al., 2023). A failure in this movement could have a repercussion on the knee by causing a dynamic recurvatum. Finally, it could also cause discomfort at the end of the swing phase when the ankle dorsiflexion contributes to start a new cycle, often by a heel strike (Hermez et al., 2023).

Several walking parameters (i.e., gait speed, cadence, stride length...), whatever the walking condition (i.e., CWS, FWS, WSDT), as well as the TUG and 6MWT deteriorated with the EDSS classes. These findings align with existing literature, which consistently confirms the significant impact of MS on walking ability (Hameau et al., 2017; Psarakis et al., 2017; Sosnoff et al., 2011). When the maximum passive amplitudes tested in the NOChU and independently of the EDSS are considered, they were generally larger than what is needed to perform daily living tasks (Fig. 1). These results suggest that the limitation of ROM does not appear to be the cause of the deficit in walking observed. Regarding the literature, when assessing the kinematics (i.e., joint movements) of walking in PwMS, the joint deflection in the lower limb is reduced, especially in knee flexion (Filli et al., 2018). Other factors appear to be responsible for this loss of joint movement, including the spasticity observed in this study; tiredness and muscle fatigability (de Haan et al., 2000); anarchic co-contraction of agonist and antagonist muscles or the individual’s cardio-respiratory condition (Benedetti et al., 1999).

The use of NOChU and gait analysis are complementary and interactive information. Despite the willingness to conduct a comprehensive NOChU, further testing could be carried out or orientated towards those joints which seemed most impacted by the MS specially the ankle. In the absence of deficits observed in most of measurements in this study in terms of ROM and strength, other tests that consider other factors, such as muscle fatigability could also be performed in future NOChU investigations. We would advise to take a different approach to the NOChU at a different stage of MS and do this evaluation from the beginning of the disease.

From a clinical perspective, integrating the NOChU and referencing Fig. 1 in the patient’s report could significantly enhance its utility in assessing the impact of potential deficits on daily living activities. In the multidisciplinary care approach for PwMS the incorporation of physiotherapy interventions is paramount (Feys et al., 2016; Khan and Amatya, 2017). It is crucial to establish a clear correlation between the localised impairments experienced by individuals and their consequent limitations in activities and participation restrictions. The potential of these investigations extends to laying the foundation for proposing personalized treatments aimed at addressing these specific impairments. This, in turn, holds the promise of enhancing the standard of care for individuals confronting MS. Ideally, we should have both information from NOChU and walking analysis to improve decision-making.

It is crucial to underscore certain limitations inherent in the study, such as testing for spasticity in more environmentally conditions, such as after testing walking or other activity of daily living. A second aspect would be in relation to using some measuring instrument to assess the sensation of fatigue. Since this is an important and recurring complaint among patients. Furthermore, investigate the impact of changes in NOChU and walking disorders on patient’s perception of quality of life. Therefore, the entire rehabilitation process should focus on this aspect, since this is what really matters to the patient.