The effect of fatigue on postural control in individuals with multiple sclerosis: A systematic review

doi:10.21203/rs.3.rs-2982487/v1

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The effect of fatigue on postural control in individuals with multiple sclerosis: A systematic review

https://doi.org/10.21203/rs.3.rs-2982487/v1

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Background: Fatigue is the most disabling ‎symptom for individuals with multiple ‎sclerosis which can significantly affect postural control by impairing the ability of the central nervous system to modulate sensory inputs and coordinate motor responses. This systematic review aimed to accumulate the existing evidence. This systematic review aimed to investigate the effect of ‎fatigue on postural control in individuals with multiple ‎sclerosis.‎

Methods: This systematic review was performed in compliance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement and registered in PROSPERO with ID CRD42022376262‎. Web of Science, PubMed, Scopus, and Google Scholar was systematically searched until January 2023, and a manual search was performed using the reference lists of included studies. Two authors independently selected the studies, extracted data, and evaluated their ‎methodological quality using the Downs and Black checklist. The process was later discussed ‎with a third author.‎

Results: Five studies were included in this review, of which consistent evidence investigating a direct ‎relationship between fatigue and ‎postural control in individuals with multiple ‎sclerosis. All the studies reported negative effects on postural control. Four ‎studies executed walking tests as fatigue protocols, and one study used a strength testing protocol for both legs, which served as a fatigue-inducing activity‎.

Conclusions: The available evidence suggests that individuals with multiple ‎sclerosis may experience postural control deficits due to fatigue. However, the present body of literature exhibits limitations in terms of its quality and methodology. Gender differences, balance, fatigue task, and muscle function are important factors that need to be taken into account when investigating the relationship between fatigue and postural control deficits in MS. Further high-quality research is necessary to comprehend the complex interplay between MS-related fatigue and postural control deficits after physical activity.

Demyelinating Diseases

Disseminated Sclerosis

Balance

Lassitude

Exhaustion

Multiple sclerosis (MS) is the most prevalent progressive and chronic disabling ‎neurologic disease that affects the central nervous system through demyelination, ‎inflammation, and axonal loss (1, 2). Brain volume loss, impaired nerve ‎conduction, and dysfunction of neural pathways are some of the MS consequences ‎‎(3). Epidemiology surveys have shown that this neurologic disease has increased to ‎‎2.8 million people worldwide in 2020 (4). This disease impacts life and is ‎a significant health problem affecting individuals’ physical, emotional, social, and cognitive functioning (4, 5). MS has many symptoms which vary according ‎to the affected region, such as cerebellar, motor, sensory, emotional, sexual, and ‎elimination-related symptoms (6). Fatigue has been identified as a major concern for individuals diagnosed with multiple sclerosis, with up to 50–60% of patients experiencing this symptom (6). In addition to the limitation in MS individuals’ activities of daily living ‎and social lives from fatigue, it also hurts cognitive functions, ‎decreasing attention and concentration (7). In some disorders like MS, fatigue may be associated with motor and/or mood disorders, so it is challenging and sometimes impossible to determine whether fatigue is an aspect of these features or a symptom (8). Fatigue physiologically is defined as “the ‎inability of a muscle or group of muscles to sustain the required or expected force” ‎by Bigland-Ritchie et al (9). Fatigue may occur from failure at force-generating ‎capacity within the muscle itself (peripheral fatigue), or because of a disability to ‎maintain the central drive to spinal motor neurons (central fatigue) (8).

Also, impaired balance, following slowed somatosensory conduction and impaired central integration is often the initial symptom of MS (10), and cause abnormal gait ‎control, and many fall frequently (11, 12, 13, 14, 15). In this aspect, MS can potentially impact the entire central nervous system, resulting in varied impairments in neurological functions (12). The integration of various sensorimotor modalities, including visual, vestibular, and proprioceptive information, plays a significant role in postural control (PC) and sustaining an upright stance (16, 17). These complex sensorimotor processes contribute to the regulation of body sway and facilitate coordinated movement patterns that maintain the center of mass within the limits of stability. Therefore, understanding the interplay between different sensory inputs and their contribution to postural control is crucial for the development of interventions aimed at improving balance and preventing falls in vulnerable populations (16, 17). Many people with MS have ‎impairment in some if not all of these processes. As a result, individuals with MS ‎showed weaker PC indicated by greater amounts of postural sway in ‎comparison to healthy controls (12, 13, 18, 19).

According to a recent systematic review study, individuals with multiple sclerosis experienced a positive impact on their fatigue levels as a result of sensory integration-based interventions. This led to improved balance and an overall increase in their quality of life. These findings may have important implications for managing symptoms and improving outcomes for individuals with MS (20). Also, brain ‎structural and functional alterations are seen in multiple sclerosis-related fatigues ‎‎(21). Particularly, ‎sensorimotor network impairment and abnormal activation of the thalamus are associated with fatigue.

To date, no systematic review has synthesized the available ‎data on the effect of fatigue on the PC of individuals with MS. By providing a comprehensive evaluation of existing research, this review aimed to address this ‎knowledge gap and shed light on the relationship between fatigue and PC in this population.

This systematic review protocol was developed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement (22) and was registered in the International Prospective Register of Systematic Reviews (PROSPERO) with registration number: CRD42022376262.

Search strategy

The relevant studies were identified through a systematic computerized search in Web of Science, PubMed, Scopus, and Google Scholar from 1st January 1974 until 1st January 2023. Two authors independently (M.A. and F.H.) searched four electronic databases. Any disagreement between the two authors was resolved by discussion and‎ a third author’s opinion (P.S.) ‎until a consensus was reached.‎ The search strategy included MeSH terms and text words for a comprehensive search. Three sets of entry strings were mixed with ‘AND’ to produce the following syntax‎: ‎("postur*" OR "postural control" OR "postural sway" OR "postural ‎stability" ‎OR ‎‎"postural ‎steadiness" OR balance OR equilibrium OR sway) ‎AND ‎‎(fatig* ‎OR ‎lassitude OR exhaustion) AND ("multiple sclerosis")‎. Restrictions applied were human studies and full-text articles. Also, the reference lists of included studies screening and a grey literature search were performed to identify additional eligible studies. Retrieved studies were transferred into Endnote and duplicates were deleted. The specific search strategy for each database is presented in Table 1.

Table 1

Search strategy
Database	Search string
Web of Science	‎("postur" OR "postural control" OR "postural sway" OR "postural ‎stability" ‎OR ‎‎"postural ‎steadiness" OR balance OR equilibrium OR sway) ‎AND ‎‎(fatig ‎OR ‎lassitude OR exhaustion) AND ("multiple sclerosis")‎
PubMed	‎("postural control"[Title/Abstract] OR "postural sway"[Title/Abstract] OR ‎‎"postural ‎stability"[Title/Abstract] OR "postural steadiness"[Title/Abstract] ‎OR balance[Title/Abstract] OR ‎equilibrium[Title/Abstract] OR ‎sway[Title/Abstract]) AND (fatigue[Title/Abstract] OR ‎lassitude[Title/Abstract] OR ‎exhaustion[Title/Abstract]) AND ("multiple ‎sclerosis"[Title/Abstract]) AND ((fft[Filter]) AND (humans[Filter]))‎
Scopus	TITLE-ABS-KEY("postur" OR "postural control" OR "postural sway" OR "postural ‎stability" OR "postural ‎steadiness" OR balance OR equilibrium OR sway) AND TITLE-ABS-KEY(fatig OR lassitude OR exhaustion‎) AND TITLE-ABS-KEY("multiple ‎sclerosis")

Eligibility Criteria and Screening Methods

Following the search process, two authors (M.A. and F.H.) independently screened all titles and abstracts generated by the search procedure. Studies were selected according to the inclusion and exclusion criteria based on Population, Intervention, Comparison, and Outcome (PICO framework) (23), as ‎mentioned in Table 2‎.

Table 2

Eligibility criteria based on PICO
	Inclusion criteria	Exclusion criteria
Population	• Individuals with multiple sclerosis • Any sex • Any age	• Any surgery affecting the lower extremities or the spine in clinical history
Intervention	• Prolonged and/or exhaustive activity organized to lead to fatigue	• No postural control measured
Comparison	• Passive control groups or conditions	• Did not include a group or conditions as comparators for quantifying fatigue following the intervention
Outcome	• Studies investigating a relationship between fatigue and postural control (must include one of the following measures: center of pressure, the center of gravity, the center of mass, and other functional scales of postural control)	• Studies not investigating a direct relationship between fatigue and postural control

Data Extraction

The two reviewers (M.A. and F.H.) independently extracted data (if available) from eligible studies and verified it by another (P.S.) Study details (author, year of publication, type of study), demographic variables of the participants (sample size, age, gender), disability ‎level, fatigue ‎protocol, conditions in which PC ‎was assessed, PC measures, key findings, and conclusion were extracted. When some necessary information was not provided in the paper, corresponding authors were contacted via email (up to three times) to obtain the requested data.

Quality assessment

Since this review included different types of articles, two authors (M.A. and F.H.) independently assessed the quality of evidence of the studies using the criteria proposed by ‎Downs and Black checklist (24), as this checklist is the best option to evaluate the quality and risk of bias for both randomized and non-randomized controlled trials (25). The checklist included 27 questions grouped into 5 categories‎ including reporting (10 items), external validity (3 items), bias (7 items), confounding (6 items), and power (1 item). The item of power (item 27) was modified to a simpler item based on the presence (score 1) or absence (score 0) of the sample size calculation. With this alternation, the best possible score is 28. The quality of induced studies consists of the following score ranges: excellent (26–28), good (20–25), fair (15–19), and poor (≤ 14). This modification‏ ‏was done in previous reviews ‎related to MS (20, 26). An opinion of a third author (P.S) was taken if a disagreement arose.

Data synthesis

A narrative data synthesis was performed. For complete reporting and transparency in the manuscript, this systematic review followed the PRISMA statement (22) and due to the different fatigue protocols and outcomes, meta-analysis was not possible. This was conducted by Synthesis Without Meta-analysis (SWiM) reporting guideline (27).

Study Identification

The electronic databases search process is presented as a flow diagram (Fig. 1) based on the PRISMA guideline (22). The search strategy retrieved 2136 articles through manual search. After removing duplicates, 1308 studies remained for further screening according to the ‎ ‎inclusion and exclusion criteria (Table 2)‎. Only five studies successfully met eligibility criteria and entered the‎ quality assessment phase.

Study Characteristics

All reviewed articles were published between 2010 and 2023 and written in English. 120 individuals participated in these studies.‎ Three out of five studies were performed without a comparison group (28, 29, 30). In four studies (28, 29, 30, 31), both sexes were included, whereas in one study (32) only female individuals were included. The mean age of the participants ‎was 46.6 years (SD 9.9), and 35% of the participants were male. Table 3 summarises the specific characteristics and retrieved data of all five studies.

Outcomes

All the studies included in the review (29, 33, 34, 35, 36), reported negative effects on PC. Four studies (29, 33, 34, 35) executed similar fatigue protocols (walking tests), and one study (36) used a strength testing protocol for both legs, which served as a fatigue-inducing activity. The following procedures for fatigue for PC assessment in four studies (29, 33, 34, 36) were performed with eyes closed ‎and eyes open. Drebinger et al. (33) explored fatigue effects on PC using visual perceptive computing. Jallouli et al. (34) examined the effect of a fatiguing task by using a stabilometric platform. Sanni et al. (29) evaluated the relationship between fatigue and following balance assessment with a force plate. Karpatkin et al. (35) investigated a direct relationship between fatigue and ‎PC by performing the Berg balance scale ‎test. Emmerik et al. ‎(36) investigated the changes in balance at different levels of self-reported fatigue.

Quality assessment

The quality assessment results ranged from 13 to 16 (Mean: 14.8), presented in Table 4. Perfect agreement between authors across the 27 items with‎ the Cohen’s kappa value 1 (0-0.20, poor agreement; 0.21–0.40, fair‎ agreement; 0.41–0.60, moderate agreement; 0.61–0.80,‎ good agreement; and 0.81-1.00, perfect agreement) (37) was obtained. All studies reported the aims, main outcome measures, participant characteristics, and probability values. Regarding the external validity, bias, and confounding items of the checklist, studies didn’t provide any information on the participants blinding to intervention, outcome assessors blinding, analysis adjusts for different lengths of follow-up of participants, allocation concealment, adjustment for confounding variables in the main analysis ‎and adjustment for loss to follow-up in the main analysis. Only, one study reported sample size calculation (28).

Table 3 Characteristics of included studies.

Study

Type of study

Participants (Number, gender, age) ‎

Disability level

Fatigue protocol

‏Outcome measures (unit)

Measurement position

Main outcomes

Conclusion

Drebinger et al. (2020)

Longitudinal

Number: 43 (Women = 20, Men = 23)

Age: 48.6 (13.7)

EDSS: 1-6

6 min of walking

Sway closed stance eyes open angular speed (degrees/s), Sway closed stance eyes closed angular speed (degrees/s), Romberg ratio angular speed (-)

Static balance function performance in eyes open and eyes closed conditions

Postural sway with closed eyes (P<0.05)

Postural sway with open eyes (P<0.05)

Romberg ratio (P>0.05)

Postural sway will increase after 6 min of walking.

Jallouli et al. (2022)

Cross-sectional

Number: 18 (Women = 11, Men = 7)

Age: 30.7 (8.2)

EDSS: 0-4

3 sets of 5 repetition sit-to-stand test

Six-minute walk test

3 sets of 5 repetition sit-to-stand test

Mean COP velocity (mm/s), COP sway area (mm²)

Bipedal and unipedal postural balance performance in eyes open and eyes closed conditions

COP velocity (P<0.01)

COP sway area (P<0.01)

Fatiguing task negatively affected postural control.

Sanni et al. (2021)

Cross-sectional

Number: 6 (Women = 3, Men = 3)

Age: 47.4 (no data)

PDDS: 3-5

6 minutes treadmill walk

COP ellipse sway area with eyes closed and eyes open (mm²)

Static balance with eyes closed and eyes open

69% increase

in the COP ellipse sway area with eyes opened (Cohen’s D 0.5)

20% increase in the COP ellipse sway area with eyes closed (Cohen’s D 0.2)

Six minutes of self-paced walking worsened balance

among people with MS.

Karpatkin et al. (2013)

Longitudinal

Number: 29 (Women = 20, Men = 9)

Age: 52.0 (8.8)

EDSS: 1.5-6

6-minute walk

Berg balance scale score (-)

Static balance with eyes open

BBS (P<0.001)

Fatigue alters the performance of people with MS on the BBS.

Emmerik et al. (2010)

Cross-sectional ‎

Number: 24 ‎‎(Women = 24, Men ‎‎= 0)‎

Age: 53.9 (8.9)‎

EDSS: 2-6

Strength testing for both legs (Peak knee extensor and dorsiflexor isometric torque and isotonic power)

Loading asymmetry (%), medial–lateral COP displacement (mm), anterior–posterior COP displacement (mm)

Static (with eyes open and eyes closed) and dynamic balance

COP loading asymmetry (P>0.05)

COP anterior displacement (P<0.05)

COP posterior displacement (P>0.05)

COP lateral displacement (P>0.05)

Additional fatigue in the MS group did affect postural control in the more challenging balance conditions.

Abbreviations: MS: multiple sclerosis, EDSS: expanded disability status scale, PDSS: promising patient-reported outcome, COP: center of pressure, mm: millimeter, S: second, BBS: ‎berg balance scale.‎

Table 4 Quality assessment of included studies.‎

‎ Article	Downs and Black checklist item																																Total (0-28)
‎ Article	Reporting											External validity				Bias								Confounding						Power			Total (0-28)
	1	2	3	4	5	6	7	8	9	10	11		12	13	14		15	16	17	18	19	20	21		22	23	24	25	26		27
Drebinger et al. (2020)	1	1	1	1	2	1	1	0	0	1	1		1	0	0		0	1	0	1	1	1	1		0	0	0	0	0		0	16
Jallouli et al. (2022)	1	1	1	1	1	1	1	0	0	1	1		1	0	0		0	1	0	1	1	1	1		0	0	0	0	0		1	16
Sanni et al. (2021)	1	1	1	1	1	1	0	0	0	1	0		1	0	0		0	1	0	1	1	1	1		0	0	0	0	0		0	13
Karpatkin et al. (2013)	1	1	1	1	1	1	0	0	0	1	0		1	1	0		0	1	0	1	1	1	1		0	1	0	0	0		0	15
Emmerik et al. (2010)	1	1	1	0	1	1	1	0	0	1	0		1	0	0		0	1	0	1	1	1	0		1	1	0	0	0		0	14

Notes: 2, criterion fully met (item 5); 1, criterion met or partially met (item 5); 0, criterion not met.

Downs and Black checklist item descriptions: 1, hypothesis/aims/objectives reported; 2, main outcome measures reported; 3,participant characteristics reported; 4, intervention details reported; 5, principal confounders reported; 6, main findings reported; 7, variability in main outcomes reported; 8, adverse events reported; 9, loss to follow-up reported; 10, probability values reported; 11, source population representative of entire population; 12, study population representative of source population; 13, study setting representative of usual care; 14, participants blinded to intervention; 15, outcome assessors blinded; 16, no retrospective subgroup analysis; 17, analysis adjusts for different lengths of follow-up of participants; 18, statistical tests are appropriate; 19, reliable compliance with intervention; 20, outcome measures are valid and reliable; 21, recruitment of study groups from same population; 22, recruitment of participants over same period;23, randomization of participants; 24, allocation concealment; 25, adjustment for confounding variables in main analysis; 26, adjustment for loss to follow-up in main analysis; 27, inclusion of sample size calculation.

This systematic review aimed to investigate whether there is a relationship between fatigue and PC in individuals with MS. The current literature on the impact of fatigue on PC in individuals with MS is limited. Tasks that induce fatigue have been shown to negatively affect PC in individuals with MS. (28, 29, 30, 31, 32). This observation is consistent with previous research highlighting the negative impact of fatigue on various aspects of motor function in individuals with MS. There are several possible reasons for this finding which will be argued in the next paragraphs.

By reviewing the methodological quality of included studies, a large amount of lack of loss to follow-up was noted (28, 29, 30, 31, 32), and may not have distinguished all achievable causes of missing follow-up data which entailed a risk of bias. Also, while this was an exploratory study and we evaluated factors that predicted loss to follow-up, it is still possible that bias may have been introduced due to loss to follow-up. Additionally, it is important to note that all of the included articles in our systematic review lacked blinding (28, 29, 30, 31, 32). Lack of blinding in a study can introduce biases in various ways, depending on who remains unblinded among the study's participants. Individuals assigned to the experimental group may have more positive expectations or report better outcomes to appease treatment providers, whereas those in the control group may have lower expectations and report poorer outcomes (38). Thus, implementing blinding protocols where possible in research studies examining fatigue in MS can improve the quality and reliability of study results.

Furthermore, all of the included studies identified other factors that may contribute to PC impairment ‎in individuals with MS, such as gender differences (34) and lower leg muscle function (29). These factors ‎should be considered when assessing PC in individuals with MS, as they may ‎require different management strategies.‎

Drebinger ‎et al. ‎(33) explored the relationship between fatigue and motor exertion on PC, indicating that ‎individuals with MS who exert more effort to perform a task may experience greater fatigue and ‎impaired PC. Jallouli et al. (34) investigated gender differences and fatiguing tasks ‎on PC and found that female ‎participants had a higher fall risk and lower functional ‎mobility than male participants. Also, several studies have suggested that women may experience higher levels of fatigue compared to men (39, 40, 41), but conflicting results have also been reported (42). This ‎suggests that gender differences should be considered when ‎assessing PC in ‎individuals with MS, and management strategies may need to be ‎adapted for female individuals.

Sanni et ‎al. ‎(29) examined the contribution of lower leg muscle function to gait and balance impairment after a ‎six-minute walk in people with MS. The findings indicate that lower leg muscle function is a ‎significant predictor of gait and balance impairment in individuals with MS. This highlights the ‎importance of considering lower leg muscle function when assessing and managing postural ‎control in individuals with MS, as strengthening exercises for the lower leg muscles may ‎improve PC and reduce falls. In contrast, a systematic and meta-analysis conducted by Rooney et al. (43) concluded that the correlation between muscle strength and fatigue was found to be neither significant nor clear. This suggests the need for further investigation to explore the potential link between these two important factors.

Karpatkin et ‎al. ‎(35) investigated the effect of fatigue on performance on the Berg Balance Scale in individuals with ‎MS. The results indicated that fatigue significantly impaired performance on the Berg Balance ‎Scale. This suggests that fatigue should be considered in assessing and managing ‎PC in individuals with MS, and alternative measures or adjustments to the scoring ‎criteria may be needed for individuals with MS who experience fatigue. In this regard, Mohebbirad et al. (20) conducted a study on the effects of exercise therapy techniques for sensory integration interventions on the lifespan of MS patients. The results showed significant improvement in balance among these individuals.

In a study conducted by Emmerik et al. (36), the effects of task, vision, and symptomatic fatigue on PC were investigated in women with MS. Results revealed that symptomatic fatigue significantly impacts PC in individuals with MS. In such cases, incorporating visual feedback as a strategy could prove to be beneficial. However, while visual feedback improves movement, it may not be as immediate as proprioceptive feedback, which can lead to instability. Therefore, incorporating proprioceptive feedback or utilizing feedback based on the limb's spatiotemporal characteristics in a neurorehabilitation system can assist patients in performing more natural movements (44). This highlights the importance of considering symptomatic ‎fatigue in assessing and managing PC in individuals with MS.

In conclusion, the current literature suggests that fatigue can negatively impact PC in individuals with MS. However, there is a lack of high-quality studies in this area, and factors such as gender differences, balance, fatigue task, and muscle function should also be considered when assessing PC in individuals with MS. Blinding protocols and alternative measures or adjustments to assessment criteria may be needed for individuals experiencing fatigue. Incorporating visual and proprioceptive feedback through neurorehabilitation systems could also prove to be beneficial. Additional research is required to investigate the clear correlation between fatigue and PC and enhance our comprehension and treatment of PC deficits among individuals with MS.

MS Multiple Sclerosis

PC Postural Control

Acknowledgments

The authors express their deepest gratitude to the reviewers for the valuable and insightful feedback provided.

Authors’ contributions

The study's conception and design were a collaborative effort among all authors. The manuscript's first draft was written by MA and FH, and they received feedback from all authors on previous versions of the manuscript. MA and FH participated in implementing the search strategy, applying the inclusion/exclusion criteria, and quality scoring system. The final version of the manuscript was read and approved by all authors.

Funding

No funding was obtained for this study.

Data Availability

The datasets generated for the current study are available on request from the corresponding author.

Declarations

Ethics approval and consent to participate

As this systematic review did not involve any participants, research ethical approval was deemed unnecessary.

Consent for publication

Not applicable.

Competing interests

The authors, Parisa Sedaghati, Mohammad Alghosi, and Freshte Hosseini, declare no competing interests that could potentially impact the content of this article.

Author details

Department of Sports Injury and Corrective Exercises, Faculty of Physical Education & Sport Sciences, University of Guilan, Rasht, Iran.‎

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No competing interests reported.

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The effect of fatigue on postural control in individuals with multiple sclerosis: A systematic review

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Abstract

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Background

Methods

Search strategy

Eligibility Criteria and Screening Methods

Data Extraction

Quality assessment

Data synthesis

Results

Study Identification

Study Characteristics

Outcomes

Quality assessment

Discussion

Conclusion

Abbreviations

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Version 1