Background
Multiple sclerosis (MS) is an inflammatory immune-mediated disease of the central nervous system (CNS) [
1‐
3]. MS affects about 2.8 million people worldwide [
4], and in 2018 its incidence was 40.4/100,000 of the population in the Kingdom of Saudi Arabia (KSA) [
5]. It is more common in young adults aged 20–40 years of age [
6] and in women than men (ratio 2:1) around the world, including in Saudi Arabia [
4].
The most common clinical manifestations of MS are numbness, urinary/bowel symptoms, ataxia, tremor or dysmetria, visual disturbance, cognitive impairment (CI), and motor dysfunction (MD) [
3,
7,
8]. Motor and cognitive dysfunction are the most common complications in patients with MS that negatively impact their quality of life (QoL) [
9‐
11].
The MD seen in MS can take several forms including mobility problems, muscle weakness, spasticity, motor incoordination, and balance dysfunction [
8,
12]. About 41% of patients with MS have walking difficulties that increase the fall risk and affect their daily living [
13‐
15].
CI is also common in patients with MS, with a reported prevalence ranging between 43% and 70% [
16‐
18]. It varies in severity and presents in all types of MS [
19]. The most affected domains of CI are executive dysfunction, lack of attention, loss of memory, and slow information processing [
20‐
22]. CI may disturb social interactions, work participation [
23], and daily living in patients with MS [
15,
24].
Understanding the relationship between motor and cognitive impairments is crucial to designing appropriate treatment plans that consider the patient’s unique symptom profile and that provides holistic care relevant to the success of physical therapy. In general, physical therapists do not give adequate attention to cognitive assessment in clinical practice. However, practitioners must be aware that the clinical assessment of cognitive function is no less important than a physical assessment of patients with MS, because it helps to determine the site of impairment and its relationship with physical abilities [
21,
25,
26].
Previous studies have shown that there is a relationship between MD and CI in other neurological diseases, such as Alzheimer’s and Parkinson’s disease [
27‐
29]. To date, similar previous studies on multiple sclerosis have focused on examining the relationship between motor and cognitive deficits [
10,
21,
25,
30‐
34] and its negative effect on the overall functioning of MS adults [
15]. Moreover, a retrospective study has revealed a significant correlation between cognitive function and a decrease in walking speed and an increase in the frequency of falls in patients with MS. However, these findings about walking speed were documented by nurses in the clinic visit and also the data of the repetition of falls were self-reported by patients or/and their family members based on their memory of the recent falls [
34]. In addition, an observational pilot study reported that recurrent fallers have higher CI compared to single-time fallers among elderly people with MS [
22]. While most studies focus on cognitive impairment as a predictor of the risk of fall, walking speed [
34], gait variability [
35], and postural control [
32], it remains unclear whether the muscle strength, motor coordination, balance, gait, and/or risk of fall can be considered as predictors of CI in adults with MS.
Therefore, the aims of this study were to: (1) investigate the association between CI and muscle weakness, motor incoordination, poor balance, gait abnormality, and high fall risk in patients with MS; and (2) examine if muscle weakness, motor incoordination, poor balance, gait abnormalities, and/or increased fall risk can be adopted as the best indicator of CI in patients with MS.
Discussion
The results of this study showed that CI is significantly associated with motor incoordination of the upper and lower extremities, balance deficits, gait abnormalities, and fall risk. However, there was no significant association between cognition and muscle strength, as estimated by hand grip and knee extension strength. Moreover, reduced upper and lower extremity coordination scores and lower fall risk were associated with higher CI scores. Specifically, the fall risk and upper extremity incoordination scores were predictive of CI in MS patients.
The results confirmed that the mean total MoCA score indicated mild cognitive impairment and in about two thirds of patients with CI, consistent with previous studies [
52,
53]. Moreover, several studies have shown that the most affected cognitive domains in MS patients were memory, abstract/conceptual reasoning, information processing, attention, and visuospatial skills [
26,
54]. Similarly, we found that memory, visuospatial skills, executive function, attention, and language were affected in patients with CI based on the MoCA scale.
This study found no association between isometric knee extensor strength and CI. Conversely, a recent study reported a significant correlation between CI and knee extension strength in MS patients [
33]. Sandroff et al. [
55] reported that the peak torque of knee extension was associated with cognitive processing speed but not verbal and visuospatial learning and memory in 62 people with MS. These contradictory results might be due smaller sample sizes or the type of dynamometer used. Similar to other studies, there was no correlation between hand grip strength and CI as measured by the total MoCA score [
33], but there was a significant correlation between hand grip strength and the language and attention domains.
The current study revealed significant correlations between motor incoordination of the upper and lower extremities and CI in patients with MS. Poor performance on rapid alternating movement and heel-to-knee tests is usually due to cerebellar dysfunction [
56]. Furthermore, several studies have shown that the cerebellum plays an important role in both the cognitive and motor functions of MS patients [
56‐
58]. This might be because the cerebello-cerebral network, consisting of the forward cortico-ponto-cerebellar pathway and the backward cerebello-thalamo-cortical pathway, also modulates cognition [
59,
60].
A balance component of POMA was significantly moderately correlated with cognitive performance in MS patients. This is the first study examining the association between cognition and balance in patients with MS using the POMA-B scale. Alfonso et al. [
61] similarly concluded that cognitive impairment in adults with MS including processing speed deficit was associated with difficulty selecting appropriate corrective movements to compensate for balance disturbances. This speculation is consistent with a previous study that found postural control becomes more difficult in MS individuals due to somatosensory and visual input deficits. Consequently, additional compensatory mechanisms are needed to overcome this postural instability which also requires the support of several cognitive domains [
62]. Moreover, other studies have examined postural–cognitive interference by incorporating the dual-task paradigms in healthy people and those with MS [
63,
64]. A recent review concluded that patients with MS showed impaired balance when they simultaneously performed a cognitive and postural task, which increased their fall risk in most daily activities [
63].
The gait component of the POMA was moderately positively correlated with cognition, consistent with previous studies demonstrating a significant association between gait abnormalities and cognitive decline in people with MS [
31,
35]. A previous study reported that step length and step time variabilities were associated with cognitive processing speed in MS patients [
31]. It is interesting to note that no study used POMA-G for the assessment of gait and its correlation with cognition in MS individuals. The current study is, therefore, unique in its use of a simple, short, inexpensive scale that does not need specialist equipment in clinical practice.
Fall risk was significantly correlated with cognitive impairment and predicted CI in MS individuals, consistent with previous studies [
34,
65]. Moreover, a higher POMA score was associated with a decrease in fall risk, which was associated with higher MoCA scores. This is particularly important when investigating the fall risk during motor examination in patients with MS and provides a clue about the presence of cognitive impairment. Furthermore, fall frequency has been shown to be significantly correlated with general intelligence, speed of cognitive processing [
22], and executive functioning, while verbal memory was found to be a significant predictor of falls in patients with MS [
34].
This study has several limitations. The sample size was small, and further studies are required with a larger sample size to improve the robustness of regression. Most of the participants had relapsing–remitting MS which limiting the generalizability of the results on the whole MS population and future studies should involve all MS subtypes. The POMA-G used in this study is based on the examiner’s observations and is less sensitive for detecting gait abnormalities than other instruments. Therefore, future studies using advanced gait analysis systems are now needed to better detect temporal and visuospatial parameters.
Conclusions
CI is significantly associated with motor incoordination, poor balance, gait abnormalities, and increased fall risk. The fall risk and upper extremity incoordination were the best indicators of CI in patients with MS. Thus, motor assessment can provide physical therapists with clues about the presence of CI in patients with MS. In addition, incorporating coordination and balance training into the rehabilitation program may enhance cognitive functions in patients with MS, although this requires empirical testing.
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