Abstract
Multiple sclerosis is a progressive neurological disorder characterised by sensory and motor impairments. This study was conducted to investigate the relationship between lower extremity sensation, muscle strength and endurance, balance, gait, and risk of falling in patients with MS. Light touch sensation (LTS) was evaluated using the Semmes-Weinstein monofilament test (threshold: ≥2/3 correct responses). Vibration sensation was tested using a 128 Hz vibration fork. Muscle strength was measured in Newtons using a hand-held dynamometer, and core muscle endurance was assessed using a pressure biofeedback device. Static balance was assessed using the single leg stand test (SLST), dynamic balance using the Y balance test (YBT), gait by the footprint method, and fall risk using the Falls Efficacy Scale—International (FES-I). Back extensor muscle strength showed a significant correlation with non-dominant YBT performance (P = .030). Abdominal muscle strength correlated with SLST performance (eyes open/closed), while lower extremity strenght correlated with both SLST and YBT outcomes (P < .05). Gait parameters were significantly related to trunk and lower extremity strength (P < .05). Back extensors, hip flexors, gluteus maximus, and hamstring muscle strength were associated with fall risk (P < .05). Importantly, LTS showed a positive association with YBT scores and a negative association with risk of falling (P < .05). Sensory and motor factors interactively contribute to balance, gait, and fall risk in MS. To reduce the risk of falls and improve functional outcomes in MS, a targeted rehabilitation programme combining sensory and motor assessments is required.
Introduction
Multiple sclerosis (MS) is a chronic disease of the central nervous system characterised by demyelination, neuroinflammation, and axonal degeneration. It most commonly affects young adults between the ages of 20 and 50. It causes a wide variety of symptoms, including muscle weakness, sensory dysfunction, fatigue, and balance disorders.1,2 In particular, impairments in proprioception and plantar cutaneous sensation are common in MS. They are strongly associated with balance disorders and an increased risk of falls. 3 While proprioception reflects the general awareness of joint position and movement, plantar cutaneous sensation provides localised tactile input from the sole of the foot. Although distinct, both are critical and complementary components of the somatosensory system that contribute to maintaining postural stability.4,5 Reduced plantar sensation and proprioceptive impairment can disrupt the integration of afferent feedback. Consequently, maintaining both static and dynamic balance may become challenging.6,7
Balance and gait are influenced by sensory inputs, but they are also affected by motor functions such as trunk and lower limb muscle strength. Previous studies have reported that weakness in the hip and trunk muscles impairs dynamic balance, slows walking speed, and increases the risk of falls in MS.6,7 However, most of these studies have examined sensory or motor impairments separately. Studies investigating their combined effect on balance, gait, and fall risk are relatively scarce.
Falls are a significant problem in MS, with ~50% of individuals reporting at least 1 fall within a 6-month period.8,9 Therefore, understanding how sensory and motor impairments affect balance and mobility is crucial for designing targeted rehabilitation programmes.10 -12
Therefore, the aim of this study is to investigate the relationship between lower limb sensory disturbances, muscle weakness, and trunk stability in individuals with MS and their balance, gait, and risk of falling. Our hypothesis is that these factors contribute to impairments in balance and gait performance and an increased risk of falling. This approach may guide clinical rehabilitation strategies by contributing to the combined assessment of balance, gait, and fall risk, which has been addressed in a limited number of studies in the literature.12 -17
Methods
Study Design
This cross-sectional study was designed to investigate the relationships between light touch sensation, vibration sense, muscle strength and endurance, balance, gait, and fall risk in individuals with multiple sclerosis (MS). The study population comprised 29 patients who attended the Neurology Outpatient Clinic at Necmettin Erbakan Medical Faculty Hospital, had a confirmed diagnosis of MS based on the 2010 McDonald criteria, and had Expanded Disability Status Scale (EDSS) scores between 3.0 and 5.5. 18 Patient collection: May 1 to September 5, 2023. Data collection: October 1 to December 15, 2023. The study was conducted in accordance with the principles of the Declaration of Helsinki and received ethical approval from the Ethics Committee of Necmettin Erbakan University, Faculty of Health Sciences (approval no: 12029-R1). Written informed consent was obtained from all participants prior to data collection. All images belong to the author. They were not taken from anywhere else.
Participant
Based on the study by Dogru Huzmeli and Duman, it was decided to include 30 people in the study. Therefore, it was stated that 32 people could participate in the study. 19 Considering the expected correlation coefficient (r = 0.552) between gluteus maximus muscle strength and SLST in the study, this sample size provides statistical power of over 99%. This supports the reliability and significance of the results obtained.
However, during the evaluation, 3 people withdrew from the study for various reasons. Inclusion criteria were: being aged between 18 and 65 years; having a definite diagnosis of MS; an EDSS score between 3.0 and 5.5; not currently using corticosteroids or having discontinued corticosteroid use at least 3 months prior to evaluation; the absence of lower extremity orthopaedic conditions that could affect walking; and not being pregnant. All assessments were performed by the physiotherapist who conducted the study (Figure 1).
Flow chart.
Measurements
The strength of the abdominal muscles, back extensors, hip flexors, gluteus maximus, quadriceps femoris, hamstrings, tibialis anterior, and tibialis posterior muscles was assessed using the MicroFET® 2 Digital Hand Dynamometer (DHD). The MicroFET® 2 is a portable device widely used in both clinical and research settings to measure isometric muscle strength. The unit of measurement is Newton. Compared to standard isokinetic dynamometers, it has demonstrated high intra-rater and inter-rater reliability, along with strong concurrent validity. 20 It is a valid and reliable tool for assessing muscle strength in neurological populations, including patients with multiple sclerosis (MS).
The muscles included in this study—abdominal muscles, back extensors, hip flexors, gluteus maximus, quadriceps femoris, hamstrings, tibialis anterior, and tibialis posterior—were selected due to their critical roles in postural control, balance, and functional mobility. Trunk muscles contribute to core stability, which is essential for maintaining upright posture and controlling centre of mass during movement. 21 Hip and thigh muscles, including the gluteus maximus, quadriceps, hamstrings, and hip flexors are vital for propulsion, shock absorption, and controlling gait phases. 22 Additionally, the tibialis anterior and posterior muscles play a key role in ankle strategy, foot clearance, and stabilisation during dynamic tasks. Given their biomechanical and neuromuscular importance in maintaining balance and preventing falls, assessing the strength of these muscle groups in individuals with MS is essential for understanding functional limitations and developing targeted interventions (Figure 2). 23
Evaluation of muscle strength.
The endurance of the core region was assessed using the Stabilizer Pressure Biofeedback Unit. 24 Prior to the measurements, participants were instructed on how to perform the movements that activate the multifidus and transversus abdominis muscles, which are essential for lumbopelvic stability. During the assessment, the pressure level (mmHg) and the duration (seconds) for which participants could maintain the contraction were recorded. To evaluate both the transversus abdominis and lumbar multifidus muscles simultaneously, participants lay in the hook-lying position. The pressure pad was placed under the lumbar spine, aligned with the midpoint between the posterior superior iliac spines (PSIS).
Light touch sensation (LTS) was objectively assessed using Semmes-Weinstein monofilaments (SWM). The test was applied to various regions of the foot—posterior lateral, posterior medial, midfoot lateral, midfoot medial, forefoot lateral, and forefoot medial—using monofilaments of 3.61, 4.31, 5.07, and 5.18 thickness. Each monofilament was applied for 1 to 1.5 seconds with enough pressure to produce a slight bend (elastic deformation). If a participant correctly identified the monofilament in at least 2 out of 3 applications in a given area, it was considered to have been detected (Figure 3). The thinnest monofilament that was detected in each area of the foot was recorded as that area’s sensory threshold. The result was recorded as “yes” or “no.”25,26
Evaluation of foot sole sensation with monofilament and fork.
Vibration sensory assessment was performed using a 128 Hz tuning fork. The assessment was performed on the first metatarsal head, medial malleolus, lateral malleolus, and heel to determine the individual’s perception of vibration. In order for the individual to perceive the vibration, the vibration was first applied to the application points and the individual was instructed to give a warning by saying “stop” when the vibration ceased. This time was recorded in seconds using a stopwatch. Thus, the time it took to perceive the vibration was determined. Vibration perception time was considered normal if it was more than 10 seconds, decreased if it was between 1 and 9 seconds, and absent if it was <1 second. 27
The single leg standing test (SLST) is a simple, reliable, and widely used test for assessing postural control in individuals with neurological disorders, including MS, as it is sensitive in detecting balance disorders that may not be apparent during bilateral stance tasks, especially in the early or mild stages of balance disorders. 28
YBT is a balance test developed to assess the dynamic balance ability of the lower extremities and trunk stability. Participants are tested barefoot or wearing sports shoes. While standing on 1 foot on the leg to be assessed, the participant attempts to reach out with the other leg in the anterior (front), posteromedial (back-inner), and posterolateral (back-outer) directions and make contact. The test is demonstrated, and 4 attempts are made for each direction. The first 3 attempts are practice, and the last 1 is the test measurement. While standing on 1 foot, the participant extends the free leg as far as possible in the specified direction and lightly touches the ground. They then return to the starting position. Returning to the starting position without losing balance, not changing the position of the supporting foot, touching the marked spot with the tested foot in a controlled manner, ensuring that the foot makes contact with the ground without slipping, and keeping the hands on the hips (or in a fixed position as required by the rules).29,30
The footprint method was used to evaluate the parameters of the walk. Measurements were made from the footprints of individuals who were asked to walk at normal walking speeds on a 10-m powdery ground. The footprints on the first 1.5 and last 1.5 m of the 10-m walking ground were disregarded, and the footprints in the middle 7 m were taken as the criterion. Walking speed, cadence, step length, double step length, step width are the walking parameters evaluated.31,32 Falls Efficacy Scale—International (FES-I) is a measurement method used to determine fear of falling in adults. 33 The threshold value for the presence of fear of falling is 24. Scores below 24 were interpreted as no risk of falling, while scores of 24 and above were interpreted as a risk of falling.
Statistical Analysis
Statistical Package for the Social Sciences (SPSS) Windows 26.0 was used for the statistical analysis of the data obtained in this study. Descriptive statistics were presented as mean ± standard deviation for continuous variables and frequency (percentage) for categorical variables. The normality of the distribution for continuous variables was assessed using the Kolmogorov-Smirnov and Shapiro-Wilk tests. Since most variables did not meet the normality assumptions, non-parametric methods were used in the analysis. The Spearman rank correlation coefficient was used to evaluate the relationships between sensory variables (light touch and vibration), muscle strength, trunk stability, balance measurements (SLST, YBT), gait parameters, and fall risk scores. Effect sizes (r values) were reported and interpreted according to Cohen’s criteria as weak (0.10-0.29), moderate (0.30-0.49), or strong (≥0.50). Additionally, multivariate linear regression analyses were conducted to investigate the predictive value of independent variables (eg, muscle strength, sensory scores) on dependent variables such as balance outcomes and fall risk scores. The statistical significance threshold was set at P < .05.
Results
A total of 29 individuals with MS (EDSS scores: 3.0-5.5) participated in the study. Among the participants, 27 were right-dominant and 2 were left-dominant in extremity usage (Table 1).
Descriptive Characteristics.
There was a moderate level positive correlation between back extensor muscle strength and the forward reach of the non-dominant (ND) extremity in the Y balance test (YBT; Table 2). Similarly, abdominal muscle strength was positively associated with static balance performance in the single leg standing test (SLST) with eyes open and closed on the ND side.
Relationship of Back Extensors and Abdominal Muscles to Static and Dynamic Balance.
D = dominant; ND = nondominant; eo = eyes open; ec = eyes close; SLST = single leg stance test; YBT = Y balance test.
P < .05.
Lower extremity muscle strength also showed several significant correlations with balance measurements. In particular, the gluteus maximus, hip flexors, hamstrings, tibialis anterior, and tibialis posterior muscles showed positive correlations with various SLST and YBT positions. For example, the gluteus maximus (dominant), tibialis anterior (dominant and ND), and tibialis posterior (ND) muscles showed a positive relationship with dynamic balance and static single-leg stance. Conversely, the quadriceps femoris (ND) and tibialis anterior (ND) muscles showed a weak negative correlation with YBT forward reach (Table 3).
The Relationship Between Right and Left Extremity Muscles and Right and Left Static and Dynamic Balance.
es = effect size; D = dominant; ND = nondominant; eo = eyes open; ec = eyes close; SLST = single leg stance test; YBT = Y balance test.
P < .05. **P < .001.
Gait performance was associated with multiple muscle groups. Double step length was positively correlated with back extensors, gluteus maximus (D), hamstrings (D), and hip flexors (D). In contrast, walking speed was negatively correlated with abdominals, hip flexors (both sides), hamstrings (ND), and gluteus maximus (both sides). Step width was positively associated with hamstring strength on the dominant side (Table 4).
Relationship Between Gait Parameters and Muscle Strength.
D = dominant; ND = nondominant.
P < .05. **P < .001. ***P < 0.001
There were moderate negative correlations between fall risk scores and back extensors, gluteus maximus (ND), and hamstrings (D; Table 5).
Relationship Between Fall Risk Score and Muscle Strength.
D = dominant; ND = nondominant.
P < .05. **P < .001.
LTS at various foot regions demonstrated moderate level positive associations with dynamic balance performance. Specifically, stronger tactile perception in the hindfoot (medial), midfoot (lateral), and forefoot (medial and lateral) corresponded to better forward, posteromedial, and posterolateral reach scores in the YBT, especially in the ND extremity (Table 6). Several moderate positive correlations were observed between LTS and gait parameters. Double step length was associated with sensation in the lateral hindfoot (dominant), while step length was linked to medial hindfoot (ND). Cadence was positively associated with tactile sensation in the lateral midfoot and medial forefoot (ND), and negatively associated with sensation in the medial midfoot (ND; Table 6).
Relationship Between Balance, Gait Parameters With Fall Risk Score and Light Touch Sensation.
D = dominant; ND = nondominant; YBT = Y balance test.
P < .05. **P < .001.
There is a moderately significant negative correlation between the fall risk score and light touch on the hindfoot lateral (ND) in the relationship between the risk of falling and sensation (Table 7).
Summary of Muscle Strength, Sensation and Function Relationships in Individuals With MS.
A moderate negative correlation was found between fall risk score and LTS in the lateral hindfoot (ND). Additionally, vibration sensation from the lateral malleolus (dominant) was positively associated with dynamic balance, and vibration from the heel (ND) was negatively associated with fall risk scores (Table 7).
There is a moderately significant positive correlation between YBT (D) forward reaching position and vibration sensation received from the lateral malleolus (D). There is a moderately significant negative correlation between fall risk and vibration sensation received from the heel (ND).
Discussion
In this study, we found that lower extremity muscle strength and sensation affect balance, walking, and fall risk. Previous studies have shown that a decrease in plantar pressure sensation is associated with balance impairment and an increased risk of falling.34,35 Jamali et al examined the prevalence of somatosensory impairments in individuals with MS and their impact on balance. Their results indicated that proprioceptive (66.7%), tactile (60.8%), and vibration (44.9%) impairments were among the most common sensory deficits. These impairments were more frequently observed in the lower extremities (78.2%) than the upper extremities (64.1%). Consequently, somatosensory dysfunctions were identified as contributors to balance problems. 14 Similarly, Citaker et al investigated the relationship between plantar sensation and balance, and found that light touch, vibration, and 2-point discrimination—as well as 1-leg stance duration—were reduced in individuals with mild to moderate MS. These deficits were associated with impaired balance performance. 5 In a study evaluating 1-leg standing duration in patients with type 2 diabetes, Kafa et al found that LTS was positively associated with balance performance. Moreover, among the parameters used to assess subplantar pressure sensation in that study, only LTS was significantly related to balance. 36 Similarly, our findings indicated that LTS was significantly associated with dynamic balance. Earlier studies have shown that dynamic balance disorders are more obvious than static balance disorders in MS. 37 For example, Prosperini and Catelli reported that dynamic balance is more sensitive than static assessments and highlighted the importance of dynamic balance in maintaining postural stability. 38 A significant correlation was also found between vibration sensation measured at the dominant lateral malleolus and dynamic balance performance in the Y balance test (YBT; P < .05). In a study conducted by Citaker et al in individuals with MS, vibration sensation at the first metatarsal head was found to be positively associated with increased 1-leg stance duration, indicating its relevance to balance performance. 5 In our study, however, vibration sensation did not show a significant association with static balance. Nonetheless, a relationship was observed between vibration at the dominant lateral malleolus and dynamic balance performance during the forward reach task. We believe that the reason for this result differing from the literature is that static balance can be maintained more by compensatory strategies (visual/vestibular), while dynamic balance is more dependent on proprioceptive sensation.
Our study found a significant relationship between lower extremity muscle strength and Y balance test (YBT) performance. This finding is consistent with previous studies reporting that quadriceps and hip muscles contribute to dynamic balance control. For example, Cattaneo et al demonstrated that muscle weakness is associated with dynamic balance impairments and increased fall risk in individuals with MS. 28 Huisinga et al also reported that reduced lower extremity muscle strength negatively affects functional reach and walking function. 39 Considering that YBT requires both postural control and force production in the dominant extremity, the relationship between muscle strength and YBT in our study suggests that muscle capacity is important for maintaining dynamic stability. These results indicate that interventions aimed at increasing muscle strength may improve YBT performance and thereby reduce the risk of falls in individuals with MS.
In summary, our study not only confirms findings in the literature but is also one of the few studies that simultaneously assesses balance, gait parameters, and fall risk in the same sample. Furthermore, the combined examination of lower limb muscle strength and different sensory inputs allows for a more comprehensive understanding of postural control mechanisms in MS. These aspects represent an original contribution to the literature and offer clinically relevant insights for rehabilitation strategies. In addition to these findings, our study also demonstrated that gluteus maximus muscle strength was positively and significantly related to walking speed.
Our study found that gluteus maximus muscle strength was positively and significantly related to walking speed. This result supports the critical role of the gluteal muscles in pelvic stabilisation. Similarly, the literature indicates that adequate force production of the gluteus maximus, especially during the push-off phase, is one of the key factors determining walking speed, as it is necessary for faster and more balanced walking.22,40,41 Additionally, gluteus maximus muscle weakness has been associated with slow walking, increased double support time, and increased risk of falls in the literature.
Our findings indicate that lower extremity muscle strength is significantly associated with the risk of falling in individuals with MS. This result is consistent with the literature, which shows that lower extremity muscle weakness is an important factor influencing falls in different populations. For example, Moreland et al reported that lower extremity muscle weakness increases the risk of falls in older adults. 42 In particular, muscle weakness in the quadriceps, gluteal muscles, and ankle stabilisers reduces postural control and decreases walking speed. These factors make individuals more susceptible to falls. Our study supports these findings in the MS population and supports the view that muscle strengthening should be included among the mechanisms effective in fall prevention.
This study has several limitations. As with other cross-sectional designs, the findings are influenced by the specific sample characteristics and the measurement tools employed. Although this research contributes to the literature on sensory assessment in individuals with MS, the sample was limited to patients attending a single MS outpatient clinic. According to their EDSS scores, participants had mild to moderate disability. Therefore, the study did not include individuals with severe disability, those residing in institutional settings, or those experiencing a relapse during the time of assessment.
Conclusion
This study investigated the relationships between sensory function (light touch and vibration), muscle strength, and trunk endurance with balance, gait, and fall risk in individuals with multiple sclerosis (MS). The findings indicate that lower extremity muscle strength and LTS play a critical role in dynamic balance and fall risk among individuals with mild to moderate MS.
These results are consistent with previous research demonstrating that impaired plantar sensation is associated with diminished balance and an increased risk of falls. The observed correlations between muscle strength and gait parameters further emphasise the importance of addressing muscular deficits in MS rehabilitation programmes. Vibration sense was found to be associated with dynamic balance, but not with static balance. Interestingly, trunk endurance did not show significant associations with the examined outcomes, which may be attributable to the relatively low level of disability within the study sample.
Supplemental Material
sj-docx-1-inq-10.1177_00469580261422580 – Supplemental material for The Relationship of Light Touch, Vibration, Muscle Strength, and Endurance With Balance, Gait, and Falling in Individuals With Multiple Sclerosis
Supplemental material, sj-docx-1-inq-10.1177_00469580261422580 for The Relationship of Light Touch, Vibration, Muscle Strength, and Endurance With Balance, Gait, and Falling in Individuals With Multiple Sclerosis by Gülsüm Demir, Fatma Erdeo, Ali Ulvi Uca and Neslihan Altuntaş Yılmaz in INQUIRY: The Journal of Health Care Organization, Provision, and Financing
Footnotes
Acknowledgements
DeepL program was used for language editing. The authors would like to thank Fortius Pharmaceutical Health Products LTD, Turkey for sponsoring the article processing charges. Special thanks to Mr. Mustafa Türker Köse for his assistance.
Ethical Considerations
All procedures performed in the study involving individuals with MS were conducted in accordance with the ethical standards of the institutional research committee, the 1964 Helsinki Declaration and subsequent amendments, and ethical standards (approval no: 12029-R1, date: April 1, 2023).
Consent to Participate
Written informed consent was obtained from all participants prior to data collection.
Author Contributions
Conceptualisation: G.D., F.E. Methodology: G.D., F.E., A.U.U., N.A.Y. Formal analyses: F.E., A.U.U., N.A.Y. Data curation: G.D., F.E. Writing—original draft: G.D., F.E. Writing—editing: G.D., F.E., A.U.U., N.A.Y. Visualisation: A.U.U., N.A.Y. Supervision: F.E., A.U.U., N.A.Y.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Data Availability Statement
The data presented in this study can be shared with the corresponding author upon request.
Clinical Implications
Rehabilitation should include sensory testing and strengthening for lower trunk and limb muscles to improve balance and reduce fall risk.
Figures
All images belong to the author. They were not taken from anywhere else.
Supplemental Material
Supplemental material for this article is available online.