Cytokine Profile with Multiple Sclerosis Following Exercise: History
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Subjects: Rehabilitation | Immunology
Contributor:
Parisa Najafi
,
Maryam Hadizadeh
,
Jadeera Phaik Geok Cheong
,
Hamidreza Mohafez
,
Suhailah Abdullah

Multiple sclerosis (MS) is defined as an immune-mediated inflammatory, neurodegenerative, and demyelinating disease that impacts the central nervous system (CNS) in young individuals. Although there are controversies regarding the exact mechanism of disease initiation, it is well known that inflammation plays an important role in pathogenesis of the disease. Inflammation promotes neurodegeneration and demyelination, starting with plaque formation in the white matter and progressing to macrophage and T-cell aggregation in the peripheral blood circulation. As important players in inflammation, cytokines, and adipokines, the effects of post-exercise on these factors in MS patients are still in the early stages of research, and results are in doubt.

  • multiple sclerosis
  • inflammatory markers
  • demyelinating autoimmune diseases

Abstract: Multiple sclerosis (MS) is one of the most prevalent causes of nontraumatic neurological impairment in young adults. This review aims to determine the impact of exercise on cytokine and adipokine profile levels as inflammatory markers in MS patients across various exercise paradigms. We used specific keywords in PubMed, Web of Science, The Cochrane Library, and Scopus to find randomized clinical trials addressing the effects of physical activity and exercise training on inflammatory markers levels in MS patients. The majority of the research showed no considerable changes in IL-6 levels, while three studies reported declining levels after the intervention. Approximately half of the trials observed a change in TNF-α and IL-10 levels after exercise interventions, while the other half showed no meaningful changes. Other markers such as IL-17, IL-4, IL-12, adipokines, and BDNF showed fluctuations in levels. We found no universal agreement on the effects of different exercise training protocols on the serum level of inflammatory markers in patients with MS. More research is needed to fully identify the effects of exercise on cytokines in MS patients.

1. Introduction

Multiple sclerosis (MS) is defined as an immune-mediated inflammatory, neurodegenerative, and demyelinating disease that impacts the central nervous system (CNS) in young individuals [1][2]. Approximately 1 to 2.5 million people (mostly women, with a female-to-male ratio of 2:1) around the world are affected by MS [3]. A variety of genetic and environmental factors, including immune system dysregulation, central nerve demyelination [4][5], vitamin D deficiency, Epstein–Barr virus, and smoking [6], have been considered as possible etiologies of MS. Ultimately, the exact primary nature of MS pathogenesis remains unknown [7][8]. Although there are controversies regarding the exact mechanism of disease initiation, it is well known that inflammation plays an important role in pathogenesis of the disease [9]. Inflammation promotes neurodegeneration and demyelination, starting with plaque formation in the white matter and progressing to macrophage and T-cell aggregation in the peripheral blood circulation [10][11]. As important players in inflammation, cytokines [12] are proteins that are released from the bloodstream, the cerebrospinal fluid (CSF), or both, which modulate the maturation and function of immune cells [13][14].
In contrast to healthy individuals, over-secretion of T helper 1 (Th1) and proinflammatory cytokines leads to imbalanced serum levels of tumor necrosis factor (TNF-α), interferon-gamma (IFN-γ), interleukin (IL)-1, IL-2, IL-12, IL-15, IL-6, chemokine (C–X–C motif) ligand 8 (CXCL8) and CXCL13, chemokine (C–C motif) ligand 20 (CCL20), T helper 2 (Th2) and anti-inflammatory cytokines IL-4, IL-5, IL-10, and IL-13 in MS patients [7][15]. Adipokines such as leptin, a proinflammatory cytokine, and adiponectin, an anti-inflammatory mediator, are cytokines produced by adipose tissue, playing crucial roles in the progression and pathogenesis of MS [16]. In addition, secretion of proinflammatory factors is increased and secretion of anti-inflammatory cytokines is decreased in MS, which may result in intensified demyelination [7]. Recent studies demonstrated that CXCL8, TNF-α, IL-12p40, IL-15, and CXCL13 are enhanced in both CSF and blood in MS patients.

The effects of post-exercise cytokines and adipokines on MS patients are still in the early stages of research, and results are in doubt. Due to the above differences in the effect of exercise on cytokines and adipokines, this study was undertaken to comprehensively evaluate randomized clinical trials (RCTs) examining the effects of exercise on inflammatory markers that have shown moderate to large changes in PwMS. In the hopes of acquiring insight into the effects of cytokines and adipokines on the pathogenesis of MS, as well as the role of exercise, finding an alternative complementary treatment for these patients is a priority. In addition, the present research provides a systematic review of the effect of exercise on PwMS as a secondary aim of mental and physical health.

2. Materials and Methods

2.1. Literature Search Strategy

A search was independently conducted through electronic databases including Scopus, Web of Science, The Cochrane Library, and PubMed by two researchers to find studies addressing the effects of physical activity and/or exercise training on serum levels of inflammatory markers in PwMS. The search language was restricted to English and Persian. The search date was limited to studies that were published from January 2003 to April 2022. This systematic review was conducted using specific keywords such as “multiple sclerosis” AND (“exercise” OR “yoga” OR “physical endurance” OR “exercise movement techniques” OR “resistance training”) AND (“interleukins” OR “tumor necrosis factor-alpha” OR “cytokines” OR “inflammation” OR “interferons” OR “adipokines” OR “leptin” OR “chemokines”). The two reviewers conducted the searches independently and prescreened the initial stage of the study selection, including the analysis of titles and abstracts. In the second stage, the full-text studies were evaluated to select them according to the eligibility criteria. A third author was responsible for supervising the procedure and resolving any discrepancies. 

2.3. Eligibility Criteria

All RCTs that evaluated the effect of any exercise or physical activity on the serum level of inflammatory markers in MS patients were included. Cytokines, chemokines, and adipokines were among the inflammatory markers evaluated in the blood and CSF in this research. Studies included had to satisfy the following criteria: (1) RCTs if they were well described and of high-quality, with defined outcomes; (2) studies on MS patients who engage in regular physical activity; (3) research on proinflammatory and anti-inflammatory cytokines or adipokines. Moreover, studies with the following criteria were excluded from the current review: articles not in English or Persian, nonhuman trials, interventions besides supplements and medicines, absence of full-text studies, duplicate reports, reviews, studies, comments, opinion pieces, methodological reports, and conference abstracts. Figure 1 depicts the screening process.

2.4. Study Selection and Data Extraction

Data from the studies were independently collected and recorded in a Microsoft Excel database by two reviewers. Again, these processes were supervised by a third researcher. Variables extracted included the first author’s name, gender, sample size, age, disease status, Expanded Disability Status Scale (EDSS), type of exercise, duration and frequency of exercise, evaluated cytokines, a secondary outcome, type of sampling, and final results of each paper.

 

3. Cytokine Profile in Patients with Multiple Sclerosis Following Exercise

3.1. Proinflammatory Cytokines

Interleukin-6 is a myokine released when skeletal muscle contracts, and nine studies reported no change in IL-6 levels after various exercises [12][17][18][19][20][21][22][23][24]. The current review is in agreement with the findings of a previous large review [25], which reported that seven trials from eight studies did not show a statistically significant difference in IL-6 levels after exercise. A possible explanation for the observed lack of IL-6 decrease in response to exercise may be that baseline IL-6 levels are not elevated in MS patients, as would be expected with MS pathogenesis as an inflammatory disease. This hypothesis is supported by a recent systematic review, which assessed 48 articles showing that IL-6 levels in the blood and CSF of MS patients were not elevated as compared to healthy individuals [7]. It is also suggested that MS patients with high IL-6 levels be included before designing a new study to examine the effect of exercise. Moreover, because exercise causes the release of IL-6 in skeletal muscles, peritendinous tissues, and the brain [20], it may be useful for future studies to also examine IL-6 levels in the blood, skeletal muscles, and CSF after intervention. In contrast to earlier findings [25], three studies with moderate intensity and frequency demonstrated a decrease in cytokine levels after exercise [26][27][28].
TNF-α is another important proinflammatory cytokine, which was studied in 11 trials. Although this study supports evidence from previous observations [25], the majority of studies found no significant changes in TNF-α following exercise training [16][20][22][29][30][31][32], while four trials indicated lower serum levels. According to the review by Bai et al., TNF- α levels in CSF and blood are higher in MS patients. Meanwhile, the reduction in Th1 after exercise is also due to a boost in cortisol and adrenaline levels in response to physical activity, which results in a decline in TNF-α produced by Th1 cells [24][33]. Only one study observed an increase in TNF-α [21], which supports the idea of a cytokine boost in serum levels via an increase in their receptors after exercise [11][25]. The scarcity and weakness of the research, the fluctuation of TNF-α levels after exercise, and the complex role of TNF-α make it difficult to fully interpret the findings. Prior investigations recommended that increased TNF-α in the blood may have a helpful [34] or harmful [35] impact on PwMS. For example, while an increase in TNF-α in CSF and blood may be associated with the stage of blood–brain barrier dysfunction [35], it may also be associated with mild drops in disease relapses [34]. All of these contradictory findings reveal that the method of training, the timing, and the type of sampling (CSF or blood) may all have an impact on the variations of cytokine production [11][25].
IFN-γ is released by T cells and natural killer cells, which are not naturally found in the CNS. According to a recent review [7], IFN-γ levels are moderately increased in MS patients when compared to healthy individuals. Although eight studies in our review showed greater fluctuation after interventions [17][20][21][22][26][32][36], our findings support evidence from previous observations showing that IFN-γ is frequently reduced by prolonged and intense activity [11][37]. This decrease implies that physical activity can naturally decline the number of peripheral blood Th-1 cells and their ability to secrete the proinflammatory cytokine. Despite these discrepancies, our findings indicate that exercise can decline serum interferon levels and the role of IFN-γ after exercise. Nevertheless, additional research into the effects of exercise is required, taking into account the type and intensity, frequency, and duration of exercise, as well as gender.
Another proinflammatory cytokine that plays an important role in the immunopathology is IL-17, which is found in the CSF and blood of PwMS patients, with a large increase during relapses [38]. Contrary to previous expectations [11], this study showed a decrease in IL-17 serum levels, which had a beneficial impact on the amount of inflammation in PwMS patients who were in the stable/remission phase and were relapse-free for at least 2 months. Moreover, this could be related to the flow of the protocol in the intervention method. The IL-12 family has also been reported to have moderate blood and CSF levels in PwMS. However, there has been less discussion about these two cytokines in the previous literature [11][25], and our results did not show consistent changes in serum levels. As such, this information was not enough to provide a definitive assessment of the factors affecting IL-12 family levels.

3.2. Anti-Inflammatory Cytokines

IL-10 is an anti-inflammatory cytokine of the Th2 type that causes disease improvement, remission, and recovery periods in PwMS [28]. It was the third most evaluated cytokines among studies [16][17][20][22][28][29][30][31][32][39][40], with five studies finding no significant changes. Although these findings support the outcomes of previous reviews [11][25], the majority of trials showed no statistically significant changes. This outcome was reflected by Bai et al. (2019), who evaluated 24 studies and did not reveal a difference in blood serum levels of IL-10 among PwMS and healthy people. Thus, in forthcoming research, more conclusive evidence may be needed to examine IL-10 following exercise. Furthermore, as IL-6 secretion decreases, IL-10 as an anti-inflammatory marker and TNF-α as a proinflammatory marker increase and decrease, respectively [31][40], which can manage and improve MS pathogenic functions such as axonal transection and demyelination [25]. Additionally, the assessment of anti-inflammatory markers such as IL-10 is worthless without considering proinflammatory markers such as IL-6 and TNF-α after exercise. The role of IL-4 in the pathogenesis of MS has been less commonly discussed in the literature. It was evaluated in five studies, and no considerable differences were reported in cytokine levels [20][31][36]. These results corroborate the findings of many previous studies [11][25] that showed ambiguity results regarding the effect of exercise on IL-4.

3.3. Adipokines

Adipokines are cytokines that manage and drive the production of proinflammatory cytokines such as TNF-α, as well as boost inflammatory signals and plague development. Leptin was one of the first adipokines to be discovered, and adiponectin is an anti-inflammatory agent [33]. Our findings reflect the results of Negaresh et al. (2018), who discovered a link between adipokine alternation and fat mass, intensity, and exercise protocol. In general, our study and previous studies [11][25] did not present adequate results to suggest that exercise programs are useful in modifying adipokine levels in PwMS.

3.4. BDNF

Brain-derived neurotrophic factor is a CNS protein which improves mood or cognition in PwMS [41], where it was evaluated alongside other inflammatory markers. Szuhany et al. (2015) reported that regular exercise, albeit at a low intensity, can increase the level of BDNF in PwMS. In addition, it was shown that the benefits of these changes may be lower in women than in men. However, our findings do not support previous research [42]; the limited RCTs evaluated in this study were not adequate to interpret the results.

3.5. Physical and Mental Health as a Secondary Outcome

In 10 studies, mental and physical factors and inflammatory markers were measured simultaneously [16][22][23][26][27][31][36][39][43][44]. A few trials indicated a rise and decline in the concurrent accumulation of anti- and proinflammatory markers and an individual’s physical and mental functions. This finding broadly supports a systematic review [11] which indicated that an increase or decrease in anti- and proinflammatory markers was not necessarily correlated with an improvement in mental and physical factors after exercise. On the other hand, these findings may be because of the limited experimental trials performed to ascertain this correlation between inflammatory markers and mental and physical health among PwMS. There is abundant room for further progress in determining the correlation of physical and mental factors with a wider range of inflammatory markers after exercise. Furthermore, using different methodologies, such as a large sample size and a long duration, may yield different results for future research. As such, exercise may be introduced as a complementary therapy that can improve physical and mental function in PwMS.

4. Conclusions

The current review did not provide a consensus on the effects of different exercise training protocols on the serum level of inflammatory markers in patients with MS. This may be attributed to variations in the population gender, design and duration of studies, and inflammatory marker measurement protocols. Although it was indicated that acute exercise induces short-term inflammation followed by a mid-term anti-inflammatory environment, there are still many unanswered questions about the beneficial methodological flaws in the face of inflammatory factors.

This entry is adapted from the peer-reviewed paper 10.3390/ijerph19138151

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