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Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2019

Open Access 01-12-2019 | Multiple Sclerosis | Review

Immunomodulatory and anti-inflammatory effects of probiotics in multiple sclerosis: a systematic review

Authors: Mohammad Morshedi, Reza Hashemi, Sara Moazzen, Amirhossein Sahebkar, Elaheh-Sadat Hosseinifard

Published in: Journal of Neuroinflammation | Issue 1/2019

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Abstract

Multiple sclerosis (MS) is an inflammatory and autoimmune neurological disorder which leads to demyelination. Although the etiology of MS is yet to be known, it appears that regulating the immune system and suppressing inflammatory pathways may possibly have a favorable effect on the healing of this disease. Evidence suggests that probiotics consumption via gut microbiome alteration devises beneficial effects in improving immune and inflammatory responses in MS. All articles were systematically searched (in the main databases) for this paper. Two investigators independently scrutinized full texts of the potentially eligible articles. The quality of the study was evaluated using standardized tools. The methodological quality of seven studies included in this review ranged from fair to good. The findings illustrated that there were statistically significant improvements in the static and dynamic balance in patients and animals with MS. In the paper in hand, the effects of probiotics administration on immune and inflammatory markers in MS disease are evaluated. In addition, the limitations and knowledge gaps were reported while proposing a possible mechanism of probiotics therapy in modulating immune and inflammatory responses. This systematic review indicated that the probiotics could improve immune and inflammatory parameters, the cytokines and cells in MS disease. Probiotics may have efficient effects in management and treatment of MS. More studies are required to clarify the effect of supplementation with probiotics and their mechanisms in MS disease.
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Literature
1.
Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, LJAon K. Diagnostic criteria for multiple Sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69:292–302.PubMedPubMedCentralCrossRef
2.
Coyle PKJCLLiN. Symptom management and lifestyle modifications in multiple Sclerosis. Continuum (Minneap Minn). 2016;22:815–36.
3.
Mielcarz DW, Kasper LH. The gut microbiome in multiple sclerosis. Curr Treat Options Neurol. 2015;17(4):18.
4.
Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008;7(12):1139-51.
5.
Milo R, Kahana E. Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmun Rev. 2010;9:A387–94.PubMedCrossRef
6.
Ramagopalan SV, Dobson R, Meier UC, Giovannoni G. Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol. 2010;9:727–39.PubMedCrossRef
7.
8.
9.
Barnett MH, Prineas JW. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol. 2004;55:458–68.PubMedCrossRef
10.
11.
12.
Musette P, Bequet D, Delarbre C, Gachelin G, Kourilsky P, Dormont D. Expansion of a recurrent V beta 5.3+ T-cell population in newly diagnosed and untreated HLA-DR2 multiple Sclerosis patients. Proc Natl Acad Sci. 1996;93:12461–6.PubMedCrossRefPubMedCentral
13.
McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ. TGF-β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell–mediated pathology. Nat Immunol. 2007;8:1390–7.PubMedCrossRef
14.
Hashemi R, Morshedi M, Jafarabadi MA, Altafi D, Hosseini-Asl SS, Rafie-Arefhosseini SJNG. Anti-inflammatory effects of dietary vitamin D3 in patients with multiple Sclerosis. Neurol Genet. 2018;4:e278.PubMedPubMedCentralCrossRef
15.
Coles AJ, Wing MG, Molyneux P, Paolillo A, Davie CM, Hale G, Miller D, Waldmann H, Compston A. Monoclonal antibody treatment exposes three mechanisms underlying the clinical course of multiple sclerosis. Ann Neurol. 1999;46:296–304.PubMedCrossRef
16.
Agnello D, Bigini P, Villa P, Mennini T, Cerami A, Brines ML, Ghezzi P. Erythropoietin exerts an anti-inflammatory effect on the CNS in a model of experimental autoimmune encephalomyelitis. Brain Res. 2002;952:128–34.PubMedCrossRef
17.
Brinkmann V. FTY720 (fingolimod) in multiple sclerosis: therapeutic effects in the immune and the central nervous system. Br J Pharmacol. 2009;158:1173–82.PubMedPubMedCentralCrossRef
18.
Morshedi M, Valenlia KB, Hosseinifard ES, Shahabi P, Abbasi MM, Ghorbani M, Barzegari A, Sadigh-Eteghad S, Saghafi-Asl M. Beneficial psychological effects of novel psychobiotics in diabetic rats: the interaction among the gut, blood, and amygdala. J Nutr Biochem. 2018;57:145–52.PubMedCrossRef
19.
Kobayashi T, Kato I, Nanno M, Shida K, Shibuya K, Matsuoka Y, MJI O. Immunotoxicology: oral administration of probiotic bacteria, Lactobacillus casei and Bifidobacterium breve, does not exacerbate neurological symptoms in experimental autoimmune encephalomyelitis. 2010;32:116–24.
20.
Kobayashi T, Kato I, Nanno M, Shida K, Shibuya K, Matsuoka Y, Onoue M. Oral administration of probiotic bacteria, Lactobacillus casei and Bifidobacterium breve, does not exacerbate neurological symptoms in experimental autoimmune encephalomyelitis. Immunopharmacology and immunotoxicology. 2010;32(1):116-24.
21.
Hosseinifard E-S, Morshedi M, Bavafa-Valenlia K, Saghafi-Asl M. The novel insight into anti-inflammatory and anxiolytic effects of psychobiotics in diabetic rats: possible link between gut microbiota and brain regions. Eur J Nutr. 2019 1-15.
22.
23.
Jangi S, Gandhi R, Cox LM, Li N, Von Glehn F, Yan R, Patel B, Mazzola MA, Liu S, Glanz BL. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun. 2016;7:12015.PubMedPubMedCentralCrossRef
24.
Brusca SB, Abramson SB, Scher JU. Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity. Curr Opin Rheumatol. 2014;26:101.PubMedPubMedCentralCrossRef
25.
26.
27.
Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci. 2011;108:4615–22.PubMedCrossRef
28.
Cekanaviciute E, Yoo BB, Runia TF, Debelius JW, Singh S, Nelson CA, Kanner R, Bencosme Y, Lee YK, Hauser SL. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci. 2017;114:10713–8.PubMedCrossRefPubMedCentral
29.
van den Hoogen WJ, Laman JD, t Hart BA. Modulation of multiple sclerosis and its animal model experimental autoimmune encephalomyelitis by food and gut microbiota. Front Immunol. 2017;8:1081.PubMedPubMedCentralCrossRef
30.
Morshedi M, Valenlia KB, Hosseinifard ES, Shahabi P, Abbasi MM, Ghorbani M, Barzegari A, Sadigh-Eteghad S, Saghafi-Asl MJTJonb. Beneficial psychological effects of novel psychobiotics in diabetic rats: the interaction among the gut, blood, and amygdala. J Nutr Biochem 2018, 57:145–152.
31.
Wang J, Tang H, Zhang C, Zhao Y, Derrien M, Rocher E, Vlieg JE-H, Strissel K, Zhao L, Obin M. Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 2015;9:1.PubMedCrossRef
32.
33.
Ganji- Arjenaki M, Rafieian- Kopaei M. Probiotics are a good choice in remission of inflammatory bowel diseases: a meta analysis and systematic review. J Cell Physiol. 2018;233:2091–103.PubMedCrossRef
34.
Musa NH, Mani V, Lim SM, Vidyadaran S, Majeed ABA, Ramasamy K. Lactobacilli-fermented cow's milk attenuated lipopolysaccharide-induced neuroinflammation and memory impairment in vitro and in vivo. J Dairy Res. 2017;84:488–95.PubMedCrossRef
35.
Salehipour Z, Haghmorad D, Sankian M, Rastin M, Nosratabadi R, Dallal MMS, Tabasi N, Khazaee M, Nasiraii LR, Mahmoudi M. Bifidobacterium animalis in combination with human origin of Lactobacillus plantarum ameliorate neuroinflammation in experimental model of multiple sclerosis by altering CD4+ T cell subset balance. Biomed Pharmacother. 2017;95:1535–48.PubMedCrossRef
36.
Tankou SK, Regev K, Healy BC, Tjon E, Laghi L, Cox LM, Kivisäkk P, Pierre IV, Hrishikesh L, Gandhi R. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann Neurol. 2018;83:1147–61.PubMedPubMedCentralCrossRef
37.
Kleerebezem M, Vaughan EE. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol. 2009;63:269–90.PubMedCrossRef
38.
Li J, Sung CYJ, Lee N, Ni Y, Pihlajamäki J, Panagiotou G, El-Nezami H. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci. 2016;113:E1306–15.PubMedCrossRefPubMedCentral
39.
Wullt M, Hagslätt M-LJ, Odenholt I, Berggren A. Lactobacillus plantarum 299v enhances the concentrations of fecal short-chain fatty acids in patients with recurrent clostridium difficile-associated diarrhea. Dig Dis Sci. 2007;52:2082.PubMedCrossRef
40.
Valenlia KB, Morshedi M, Saghafi-Asl M, Shahabi P, Abbasi MMJJoFF: Beneficial impacts of Lactobacillus plantarum and inulin on hypothalamic levels of insulin, leptin, and oxidative markers in diabetic rats 2018, 46:529–537.
41.
Yadav H, Lee J-H, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J Biol Chem. 2013;288:25088–97.PubMedPubMedCentralCrossRef
42.
Valenlia KB, Morshedi M, Saghafi-Asl M, Shahabi P, Abbasi MM. Beneficial impacts of Lactobacillus plantarum and inulin on hypothalamic levels of insulin, leptin, and oxidative markers in diabetic rats. J Funct Foods. 2018;46:529-37.
43.
Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F. Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci. 2010;107:454–9.PubMedCrossRef
44.
Tankou SK, Regev K, Healy BC, Cox LM, Tjon E, Kivisakk P, Vanande IP, Cook S, Gandhi R, Glanz B. Investigation of probiotics in multiple sclerosis. Mult Scler J. 2018;24:58–63.CrossRef
45.
Moher D, Liberati A, Tetzlaff J, Altman DGJAoim. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. 2009;151:264–9.
46.
Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1.PubMedPubMedCentralCrossRef
47.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264-9.
48.
Higgins JP, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, Savović J, Schulz KF, Weeks L, Sterne JA. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.PubMedPubMedCentralCrossRef
49.
Viswanathan M, Berkman ND, Dryden DM, Hartling L. Assessing risk of bias and confounding in observational studies of interventions or exposures: further development of the RTI item bank; 2013.
50.
Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, et al. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin Nutr. 2016:1–24.
51.
Secher T, Kassem S, Benamar M, Bernard I, Boury M, Barreau F, et al. Oral administration of the probiotic strain Escherichia coli nissle 1917 reduces susceptibility to neuroinflammation and repairs experimental autoimmune encephalomyelitis-induced intestinal barrier dysfunction. Front Immunol. 2017;8:1–10.CrossRef
52.
Kobayashi T, Suzuki T, Kaji R, Serata M, Nagata T, Ando M, et al. Probiotic upregulation of peripheral IL-17 responses does not exacerbate neurological symptoms in experimental autoimmune encephalomyelitis mouse models. Immunopharmacol Immunotoxicol. 2012;34(3):423–33.PubMedCrossRef
53.
Kwon HK, Kim GC, Kim Y, Hwang W, Jash A, Sahoo A, et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol. 2013;146:217–27.PubMedCrossRef
54.
Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, Molin G, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):1–11.CrossRef
55.
Marteau P. Evidence of probiotic strain specificity makes extrapolation of results impossible from a strain to another, even from the same species. Ann Gastroenterol Hepatol. 2011;2:1–3.
56.
McFarland LV, Evans CT, Goldstein EJ. Strain-specificity and disease-specificity of probiotic efficacy: a systematic review and meta-analysis. Front Med. 2018;5:124.CrossRef
57.
Kajander K, Myllyluoma E, Rajilić-Stojanović M, Kyrönpalo S, Rasmussen M, Järvenpää S, Zoetendal E, De Vos W, Vapaatalo H, Korpela R. Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota. Aliment Pharmacol Ther. 2008;27:48–57.PubMedCrossRef
58.
Timmerman H, Koning C, Mulder L, Rombouts F, Beynen A. Monostrain, multistrain and multispecies probiotics—a comparison of functionality and efficacy. Int J Food Microbiol. 2004;96:219–33.PubMedCrossRef
59.
Ma X, Hua J, Li Z. Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol. 2008;49:821–30.PubMedPubMedCentralCrossRef
60.
Patel RM, Myers LS, Kurundkar AR, Maheshwari A, Nusrat A, Lin PW. Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am J Pathol. 2012;180:626–35.PubMedPubMedCentralCrossRef
61.
De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci. 2010;107:14691–6.PubMedCrossRefPubMedCentral
62.
O'Toole PW, Claesson MJ. Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J. 2010;20:281–91.CrossRef
63.
Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP. A core gut microbiome in obese and lean twins. Nature. 2009;457:480.PubMedCrossRef
64.
65.
66.
Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701.PubMedCrossRef
67.
Bull-Otterson L, Feng W, Kirpich I, Wang Y, Qin X, Liu Y, Gobejishvili L, Joshi-Barve S, Ayvaz T, Petrosino J. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One. 2013;8:e53028.PubMedPubMedCentralCrossRef
68.
Mack D, Ahrné S, Hyde L, slS, Hollingsworth M. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut. 2003;52:827–33.PubMedPubMedCentralCrossRef
69.
Forsyth CB, Farhadi A, Jakate SM, Tang Y, Shaikh M, Keshavarzian A. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol. 2009;43:163–72.PubMedPubMedCentralCrossRef
70.
Erridge C, Kennedy S, Spickett CM, Webb DJ. Oxidized phospholipid inhibition of toll-like receptor (TLR) signaling is restricted to TLR2 and TLR4 roles for cd14, lps-binding protein, and md2 as targets for specificity of inhibition. J Biol Chem. 2008;283:24748–59.PubMedPubMedCentralCrossRef
71.
Guo S, Al-Sadi R, Said HM, Ma TY. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol. 2013;182:375–87.PubMedPubMedCentralCrossRef
72.
73.
Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi J, Verschoor CP, Loukov D, Schenck LP, Jury J, Foley KP. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microbe. 2017;21:455–66 e454.PubMedPubMedCentralCrossRef
74.
Maldonado Galdeano C, Novotny Nunez I, Carmuega E, de Moreno de LeBlanc A, Perdigon G. Role of probiotics and functional foods in health: gut immune stimulation by two probiotic strains and a potential probiotic yoghurt. Endocr Metab Immune Disord Drug Targets. 2015;15:37–45.PubMedCrossRef
75.
Arora T, Bäckhed F. The gut microbiota and metabolic disease: current understanding and future perspectives. J Intern Med. 2016;280:339–49.PubMedCrossRef
76.
Conlon M, Bird A. The impact of diet and lifestyle on gut microbiota and human health. Nutrients. 2015;7:17–44.CrossRef
77.
Dave M, Higgins PD, Middha S, Rioux KP. The human gut microbiome: current knowledge, challenges, and future directions. Transl Res. 2012;160:246–57.PubMedCrossRef
78.
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559.PubMedCrossRef
79.
Metadata
Title
Immunomodulatory and anti-inflammatory effects of probiotics in multiple sclerosis: a systematic review
Authors
Mohammad Morshedi
Reza Hashemi
Sara Moazzen
Amirhossein Sahebkar
Elaheh-Sadat Hosseinifard
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2019
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-019-1611-4

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