MULTIPLE SCLEROSIS IS ASSOCIATED WITH ALTERED QUANTITATIVE AND QUALITATIVE COMPOSITION OF INTESTINAL MICROBIOTA

  • Authors: Abdurasulova IN1, Tarasova EA2, Ermolenko EI3, Eliseev AV4, Matsulevich AV5, Bisaga GN6, Skulyabin DI5, Suvorov AN3, Klimenko VM5
  • Affiliations:
    1. Institute of Experimental Medicine, St. Petersburg State Pediatric Medical University
    2. Institute of Experimental Medicine, Research laboratory «Explana»
    3. Institute of Experimental Medicine, St. Petersburg State University
    4. Research laboratory «Explana»
    5. Institute of Experimental Medicine
    6. Kirov Military Medical Academy
  • Issue: Vol 15, No 3 (2015)
  • Pages: 55-67
  • Section: Articles
  • URL: https://journals.eco-vector.com/MAJ/article/view/9674
  • DOI: https://doi.org/10.17816/MAJ15355-67
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Abstract


Recent literature raises questions about the role of intestinal microbiota in the regulation of immune functions and in supporting of chronic inflammation upon numerous neurological conditions including multiple sclerosis (MS). On the other hand, almost 70% of MS patients have gastrointestinal problems. Study objective: Analysis of the qualitative and quantitative composition of intestinal microflora in MS patients. Materials and methods: The study group included 21 patients (14 females and 7 males). Intestinal microbiota was studied using bacteriological techniques and real-time polymerase chain reaction (RT PCR). Results: All patients were found to have alterations (dysbiosis) in the compositions of intestinal microbial populations manifested as decreases in symbiotic bacteria and the appearance and excessive proliferation of conditionally pathogenic microorganisms, there being certain intersex differences between patients: women showed decreased proportions of hormone-dependent lactobacilli and the excessive proliferation of weakly pathogenic atypical Escherichia, Citrobacter and Acinetobacter species, whereas men showed high rates of detection of S. aureus, Klebsiella sp., Proteus sp., and Candida fungi. The role of intestinal dysbiosis in the pathogenesis of MS and the possibility to treat disturbances in bacterial homeostasis with probiotics are discussed.

I N Abdurasulova

Institute of Experimental Medicine, St. Petersburg State Pediatric Medical University

Email: i_abdurasulova@mail.ru
St. Petersburg, Russia

E A Tarasova

Institute of Experimental Medicine, Research laboratory «Explana»

St. Petersburg, Russia

E I Ermolenko

Institute of Experimental Medicine, St. Petersburg State University

St. Petersburg, Russia

A V Eliseev

Research laboratory «Explana»

St. Petersburg, Russia

A V Matsulevich

Institute of Experimental Medicine

St. Petersburg, Russia

G N Bisaga

Kirov Military Medical Academy

St. Petersburg, Russia

D I Skulyabin

Institute of Experimental Medicine

St. Petersburg, Russia

A N Suvorov

Institute of Experimental Medicine, St. Petersburg State University

St. Petersburg, Russia

V M Klimenko

Institute of Experimental Medicine

St. Petersburg, Russia

  1. Stys P. K., Zamponi G. W., van Minnen J., Geurts J. J. G. Will the real multiple sclerosis please stand up? // Nat. Rev. Neurosci.- 2012.- Vol. 13, № 7.- P. 507-514.
  2. Абдурасулова И. Н., Клименко В. М. Роль иммунных и глиальных клеток в процессе нейродегенерации // Медицинский академический журнал.- 2011.- Т. 1.- С. 12-29.
  3. McFarland H. F., Martin R. Multiple sclerosis: a complicated picture of autoimmunity // Nat. Immunol.- 2007.- Vol. 8, № 9.- P. 913-919.
  4. Steiner G. Acute plaques in multiple sclerosis, their pathogenetic significance and the role of spirochetes as etiological factor // J. Neuropathol. Exp. Neurol.- 1952.- Vol. 11, № 4.- P. 343-372.
  5. Stratton C. W., Wheldon D. B. Multiple sclerosis: An infectious syndrome involving Chlamydophila pneumoniae // Trends Microbiol.- 2006.- Vol. 14, № 11.- P. 474-479.
  6. Berer K., Krishnamoorty G. Microbial viuw of central nervous system autoimmunity // FEBS Letters.- 2014.- Vol. 588.- P. 4207-4213.
  7. Hill D. A., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis // Annu. Rev. Immunol.- 2010.- Vol. 28.- P. 623-667.
  8. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., Taniguchi T., Takeda K., Hori S., Ivanov I. I., Umesaki Y., Itoh K., Honda K. Induction of colonic regulatory T cells by indigenous Clostridium species // Science.- 2011.- Vol. 331, № 6015.- P. 337-341.
  9. Gaboriau-Routhiau V., Rakotobe S., Lécuyer E., Mulder I., Lan A., Bridonneau C., Rochet V., Pisi A., De Paepe M., Brandi G., Eberl G., Snel J., Kelly D., Cerf-Bensussan N. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses // Immunity.- 2009.- Vol. 31, № 4.- P. 677-689.
  10. Ivanov I.I., Frutos R.de L., Manel N., Yoshinaga K., Rifkin D. B., Sartor R. B., Finlay B. B., Littman D. R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine // Cell Host Microbe.- 2008.- Vol. 4, № 4.- P. 337-349.
  11. Ivanov I.I., Atarashi K., Manel N., Brodie E. L., Shima T., Karaoz U., Wei D., Goldfarb K. C., Santee C. A., Lynch S. V., Tanoue T., Imaoka A., Itoh K., Takeda K., Umesaki Y., Honda K., Littman D. R. Induction of intestinal Th17 cells by segmented filamentous bacteria // Cell.- 2009.- Vol. 139, № 3.- P. 485-498.
  12. Wu G. D., Chen J., Hoffmann C., Bittinger K., Chen Y.Y., Keilbaugh S. A., Bewtra M., Knights D., Walters W. A., Knight R., Sinha R., Gilroy E., Gupta K., Baldassano R., Nessel L., Li H., Bushman F. D., Lewis J. D. Linking longterm dietary patterns with gut microbial enterotypes // Science.- 2011.- Vol. 334, № 6052.- P. 105-108.
  13. Hall J. A., Bouladoux N., Sun C. M., Wohlfert E. A., Blank R. B., Zhu Q., Grigg M. E., Berzofsky J. A., Belkaid Y. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses // Immunity.- 2008.- Vol. 29, № 4.- P. 637-649.
  14. Mazmanian S. K., Liu C. H., Tzianabos A. O., Kasper D. L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system // Cell.- 2005.- Vol. 122, № 1.- P. 107-118.
  15. Ochoa-Repâraz J., Mielcarz D. W., Ditrio L. E., Burroughs A. R., Begum-Haque S., Dasgupta S., Kasper D. L., Kasper L. H. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression // J. Immunol.- 2010.- Vol. 185, № 7.- P. 4101-4108.
  16. O’Mahony C., Scully P., O’Mahony D., Murphy S., O’Brien F., Lyons A., Sherlock G., MacSharry J., Kiely B., Shanahan F., O’Mahony L. Commensal-induced regulatory T cells mediate protection against pathogenstimulated NF-kappaB activation // PLoS Pathog.- 2008.- Vol. 4, № 8.- e1000112.
  17. Round J. L., Mazmanian S. K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota // Proc. Natl. Acad. Sci. USA.- 2010.- Vol. 107, № 27.- P. 12204-12209.
  18. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L. G., Gratadoux J. J., Blugeon S., Bridonneau C., Furet J. P., Corthier G., Grangette C., Vasquez N., Pochart P., Trugnan G., Thomas G., Blottiere H. M., Doré J., Marteau P., Seksik P., Langella P. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients // Proc. Natl. Acad. Sci. USA.- 2008.- Vol. 105, № 43.- P. 16731-16736.
  19. Lee Y. K., Mazmanian S. K. Has the microbiota played a critical role in the evolution of the adaptive immune system? // Science.- 2010.- Vol. 330, № 6012.- P. 1768-1773.
  20. Westall F. C. Molecular mimicry revisited: Gut bacteria and multiple sclerosis // J. Clin. Microbiol.- 2006.- Vol. 44, № 6.- P. 2099-2104.
  21. Bäckhed F., Ley R. E., Sonnenburg J. L., Peterson D. A., Gordon J. I. Host-bacterial mutualism in the human intestine // Science.- 2005.- Vol. 307, № 5717.- P. 1915-1920.
  22. Linden J. R., Ma Y., Zhao B., Harris J. M., Rumah K. R., Schaeren-Wiemers N. S., Vartanian T. Clostridium perfringens Epsilon Toxin Causes Selective Death of Mature Oligodendrocytes and Central Nervous System Demyelination // Mbio.- 2015.- Vol. 6, № 3.- e0513-14.
  23. Mulvey M. R., Doupe M., Prout M., Leong C., Hizon R., Grossberndt A., Klowak M., Gupta A., Melanson M., Gomori A., Esfahani F., Klassen L., Frost E. E., Namaka M. Staphylococcus aureus harbouring Enterotoxin A as a possible risk factor for multiple sclerosis exacerbations // Multiple Sclerosis J.- 2010.- Vol. 17, № 4.- P. 397-403.
  24. Langer-Gould A., Albers K. B., Van Den Eeden S. K., Nelson L. M. Autoimmune diseases prior to the diagnosis of multiple sclerosis: a population based case-control study // Mult. Scler.- 2010.- Vol. 16, № 7.- P. 855-861.
  25. Zephir H., Gower-Rousseau C., Salleron J., Simon O., Debouverie M., Le Page E., Bouhnik Y., Lebrum-Frenay C., Papeix C., Vigneron B., Allez M., Prin L., Cosnes J., Vermersch P., Colombel J. F. for the CFSEP, GETAID and EPIMAD Groups. Milder multiple sclerosis course in patients with concomitant inflammatory bowel disease // Mult. Scler.- 2013.- Vol. 20, № 8.- P. 1135-1139.
  26. Frank D. N., St Amand A. L., Feldman R. A., Boedeker E. С., Harpaz N., Pace N. R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases // Proc. Natl. Acad. Sci. USA.- 2007.- Vol. 104, № 34.- P. 13780-13785.
  27. Sellon R. K., Tonkonogy S., Schultz M., Dieleman L. A., Grenther W., Balish E., Rennick D. M., Sartor R. B. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice // Infect Immun.- 1998.- Vol. 66, № 11.- P. 5224-5231.
  28. Sokol H., Seksik P., Rigottier-Gois L., Lay C., Lepage P., Podglajen I., Marteau P., Doré J. Specificities of the fecal microbiota in inflammatory bowel disease // Inflamm. Bowel Dis.- 2006.- Vol. 12, № 2.- P. 106-111.
  29. Edwards C. J. Commensal gut bacteria and the etiopathogenesis of rheumatoid arthritis // J. Rheumatol.- 2008.- Vol. 35, № 8.- P. 1477-1479.
  30. Wen L., Ley R. E., Volchkov P. Y., Stranges P. B., Avanesyan L., Stonebraker A. C., Hu C., Wong F. S., Szot G. L., Bluestone J. A., Gordon J. I., Chervonsky A. V. Innate immunity and intestinal microbiota in the development of Type 1 diabetes // Nature.- 2008.- Vol. 455, № 7216.- P. 1109-1113.
  31. Zabad R. K., Metz L. M., Todoruk T. R., Zhang Y., Mitchell J. R., Yeung M., Patry D. G., Bell R. B., Yong V. W. The clinical response to minocycline in multiple sclerosis is accompanied by beneficial immune changes: A pilot study / / Mult. Scler.- 2007.- Vol. 13, № 4.- P. 517-526.
  32. Zhang Y., Metz L. M., Yong V. W., Bell R. B., Yeung M., Patry D. G., Mitchell J. R. Pilot study of minocycline in relapsing-remitting multiple sclerosis // Can. J. Neurol. Sci.- 2008.- Vol. 35, № 2.- P. 185-191.
  33. Ochoa-Repâraz J., Mielcarz D. W., Ditrio L. E., Burroughs A. R., Foureau D. M., Haque-Begum S., Kasper L. H. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis // J. Immunol.- 2009.- Vol. 183, № 10.- P. 6041-6050.
  34. Абдурасулова И. Н., Тарасова Е. А., Мацулевич А. В., Елисеев А. В., Ермоленко Е. И., Суворов А. Н., Клименко В. М. Изменение качественного и количественного состава кишечной микробиоты у крыс в течение экспериментального аллергического энцефаломиелита // Рос. физиол. журн.- 2015.- (в печати).
  35. Berer K., Mues M., Koutrolos M., Rasbi Z. A., Boziki M., Johner C., Wekerle H., Krishnamoorthy G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination // Nature.- 2011.- Vol. 479, № 7374.- Р. 538-541.
  36. Lee Y. K., Menezes J. S., Umesaki Y., Mazmanian S. K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis // Proc. Natl. Acad. Sci. USA.- 2011.- Vol. 108, Suppl 1.- P. 4615-4622.
  37. Nessler S., Dodel R., Bittner A., Reuss S., Du Y., Hemmer B., Sommer N. Effect of minocycline in experimental autoimmune encephalomyelitis // Ann. Neurol.- 2002.- Vol. 52 № 5.- P. 689-690.
  38. Popovic N., Schubart A., Goetz B. D., Zhang S. C., Linington C., Duncan I. D. Inhibition of autoimmune encephalomyelitis by a tetracycline // Ann. Neurol.- 2002.- Vol. 51, № 2.- P. 215-223.
  39. Sriram S., Mitchell W., Stratton C. Multiple sclerosis associated with Chlamydia pneumoniae infection of the CNS // Neurology.- 1998.- Vol. 50, № 2.- P. 571-572.
  40. Yokote H., Miyake S., Croxford J. L., Oki S., Mizusawa H., Yamamura T. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora // Am. J. Pathol.- 2008.- Vol. 173, № 6.- P. 1714-1723.
  41. Ezendam J., de Klerk A., Gremmer E. R., van Loveren H. Effects of Bifidobacterium animalis administered during lactation on allergic and autoimmune responses in rodents // Clin. Exp. Immunol.- 2008.- Vol. 154, № 3.- P. 424-431.
  42. 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 // Immunopharmacol. Immunotoxicol.- 2010.- Vol. 32, № 1.- P. 116-124.
  43. Kwon H. K., Kim G. C., Kim Y., Hwang W., Jash A., Sahoo A., Kim J. E., Nam J. H., Im S. H. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response // Clin. Immunol.- 2013.- Vol. 146, № 3.- P. 217-227.
  44. Lavasani S., Dzhambazov B., Nouri M., Fâk F., Buske S., Molin G., Thorlacius H., Alenfall J., Jeppsson B., Weström B. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells // PLoS One.- 2010.- Vol. 5, № 2.- e9009.
  45. Ochoa-Repâraz J., Mielcarz D. W., Wang Y., Begum-Haque S., Dasgupta S., Kasper D. L., Kasper L. H. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease // Mucosal Immunol.- 2010.- Vol. 3, № 5.- P. 487-495.
  46. Takata K., Kinoshita M., Okuno T., Moriya M., Kohda T., Honorat J.A., Sugimoto T., Kumanogoh A., Kayama H., Takeda K., Sakoda S., Nakatsuji Y. The lactic acid bacterium Pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells // PLoS One.- 2011.- Vol. 6, № 11.- e27644.
  47. Maassen C. B., Claassen E. Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity // Vaccine.- 2008.- Vol. 26, № 17.- P. 2056-2057.
  48. Baken K. A., Ezendam J., Gremmer E. R., de Klerk A., Pennings J. L., Matthee B., Peijnenburg A. A., van Loveren H. Evaluation of immunomodulation by Lactobacillus casei Shirota: immune function, autoimmunity and gene expression // Int. J. Food Microbiol.- 2006.- Vol. 112, № 1.- P. 8-18.
  49. Ezendam J., van Loveren H. Lactobacillus casei Shirota administered during lactation increases the duration of autoimmunity in rats and enhances lung inflammation in mice // Br. J. Nutr.- 2008.- Vol. 99, № 1.- P. 83-90.
  50. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., 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. USA.- 2010.- Vol. 107, № 33.- P. 14691-14696.
  51. Piccio L., Stark J. L., Cross A. H. Chronic calorie restriction attenuates experimental autoimmune encephalomyelitis // J. Leukoc. Biol.- 2008.- Vol. 84, № 4.- P. 940-948.
  52. Kleinewietfeld M., Manzel A., Titze J., Kvakan H., Yosef N., Linker R. A., Muller D. N., Hafler D. A. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells // Nature.- 2013.- Vol. 496, № 7446.- P. 518-522.
  53. Wu G. D., Bushmanc F. D., Lewis J. D. Diet, the human gut microbiota, and IBD // Anaerobe.- 2013.- Vol. 24.- P. 117-120.
  54. Kira J., Yamasaki K., Horiuchi I., Ohyagi Y., Taniwaki T., Kawano Y. Changes in the clinical phenotypes of multiple sclerosis during the past 50 years in Japan // J. Neurol. Sci.- 1999.- Vol. 166, № 1.- P. 53-57.
  55. Levinthal D. J., Rahman F., Nusrat S., O’Leary M., Heyman R., Bielefeldt K. Adding to the burden: gastrointestinal symptoms and syndromes in multiple sclerosis // Mult. Scler. Int. Art.- 2013.- ID 319201, 9 pages.
  56. Эпштейн-Литвак Р. В., Вильшанская Ф. Л. Бактериологическая диагностика дисбактериоза кишечника: метод. рекомендации.- M.: 1977.- 22 с.
  57. Carding S., Verbeke K., Vipond D. T., Corfe B. M., Owen L. J. Dysbiosis of the gut microbiota in disease // Microb. Ecol. Health Dis.- 2015.- V 26, 26191.- 9 p.
  58. Clemente J. C., Ursell L. K., Parfrey L. W., Knight R. The impact of the gut microbiota on human health: an integrative view // Cell.- 2012.- Vol. 148, № 6.- P. 1258-1270.
  59. Arndt A., Hoffacker P., Zellmer K., Goecer O., Recks M. S., Kuerten S. Conventional housing conditions attenuate the development of experimental autoimmune encephalomyelitis // PLoS One.- 2014.- Vol. 9, № 6.- e 99794.
  60. Turnbaugh P. J., Ridaura V. K., Faith J. J., Rey F. E., Knight R., Gordon J. I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice // Sci. Transl. Med.- 2009.- Vol. 1, № 6.- 6ra14.
  61. Stecher B., Maier L., Hardt W. D. «Blooming” in the gut: How dysbiosis might contribute to pathogen evolution // Nat. Rev. Microbiol.- 2013.- Vol. 11, № 4.- P. 277-284.
  62. Winter S. E., Winter M. G., Xavier M. N., Thiennimitr P., Poon V., Keestra A. M., Laughlin R. C., Gomez G., Wu J., Lawhon S.D., Popova I. E., Parikh S. J., Adams L. G., Tsolis R. M., Stewart V. J., Bäumler A. J. Host-derived nitrate boosts growth of E. coli in the inflamed gut // Science.- 2013.- Vol. 339, № 6120.- P. 708-711.
  63. Baumgart M., Dogan B., Rishniw M., Weitzman G., Bosworth B., Yantiss R., Orsi R. H., Wiedmann M., McDonough P., Kim S. G., Berg D., Schukken Y., Scherl E., Simpson K. W. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum / / ISME J.- 2007.- Vol. 1, № 5.- P. 403-418.
  64. Ермоленко Е. И., Исаков В. А., Ждан-Пушкина С. Х., Тец В. В. Количественная характеристика антагонистической активности лактобацилл // Журн. микробиол.- 2004.- Т. 5.- С. 94-98.
  65. Marik C., Felts P. A., Bauer J., Lassmann H., Smith K. J. Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? // Brain.- 2007.- Vol. 130, Pt. 11.- P. 2800-2815.
  66. Maier E., Anderson R. C., Roy N. C. Understanding how commensal obligate anaerobic bacteria regulate immune functions in the large intestine // Nutrients.- 2014.- Vol. 7, № 1.- P. 45-73.
  67. Wing Y., Telesford K. M., Ochoa-Repâraz J., Haque-Begum S., Christy M. ,Kasper E. J., Wang L., Wu Y., Robson S. C., Kasper D. L., Kasper L. H. An intestinal commensal symbiosis factor controls neuroinflammation via TLR2-mediated CD39 signalling // Nat. Commun.- 2014.- Vol. 5, P. 4432.
  68. Hickey C. A., Kuhn K. A., Donermeyer D. L., Porter N. T., Jin C., Cameron E. A., Jung H., Kaiko G. E., Wegorzewska M., Malvin N. P., Glowacki R. W., Hansson G. C., Allen P. M., Martens E. C., Stappenbeck T. S. Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles // Cell Host Microbe.- 2015.- Vol. 17, № 5.- P. 672-680.
  69. Varela E., Manichanh C., Gallart M., Torrejon A., Borruel N., Casellas F., Guarner F., Antolin M. Colonisation by Faecalibacterium prausnitzii and maintenance of clinical remission in patients with ulcerative colitis // Aliment. Pharmacol. Ther. - 2013. - Vol. 38, № 2. - P. 151-161.
  70. Schiffenbauer J., Johnson H. M., Butfiloski E. J., Weqrzyn L., Soos J. M. Staphylococcal enterotoxins can reactivate experimental allergic encephalomyelitis // Proc. Natl. Acad. Sci. USA.- 1993.- Vol. 90, № 18.- P. 8543-8546.
  71. Brocke S., Gaur A., Piercy C., Gautam A., Gijbels K., Fathman C. G., Steinman L. Induction of relapsing paralysis in experimental autoimmune encephalomyelitis by bacterial superantigen.- Nature.- 1993.- Vol. 365, № 6447.- P. 642-644.
  72. França T. G., Chiuso-Minicucci F., Zorzella-Pezavento S. F., Ishikawa L. L., da Rosa L. C., Colavite P. M., Marques C., Ikoma M. R., da Cunha Mde L., Sartori A. Previous infection with Staphylococcus aureus strains attenuated experimental encephalomyelitis // BMC Neurosci.- 2014.- Vol. 15, 8.
  73. Kumar P., Kretzschmar B., Herold S., Nau R., Kreutzfeldt M., Schütze S., Bähr M., Hein K. Beneficial effect of chronic Staphylococcus aureus infection in a model of multiple sclerosis is mediated through the secretion of extracellular adherence protein // J. Neuroinflammation.- 2015.- Vol. 12, 22.
  74. Rumah K. R., Linden J., Fischetti V. A., Vartanian T. Isolation of Clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease // PLoS One.- 2013.- Vol. 8, № 10.- e76359.
  75. Tiwana H., Wilson C., Walmsley R. S., Wakefield A. J., Smith M. S., Cox N. L., Hudson M. J., Ebringer A. Antibody responses to gut bacteria in ankylosing spondylitis, rheumatoid arthritis, Crohn’s disease and ulcerative colitis / / Rheumatol. Int.- 1997.- Vol. 17, № 1.- P. 11-16.
  76. Лобзин Ю. В., Макарова В. Г., Кровякова Е. Р. Дисбактериоз кишечника (клиника, диагностика, лечение): руководство для врачей.- СПб.: ООО «Изд-во Фолиант», 2003.- 256 с.
  77. Airas L. Hormonal and gender-related immune changes in multiple sclerosis // Acta Neurol. Scand.- 2015.- Vol. 132, Suppl. 199.- P. 62-70.
  78. Tomassini V., Pozzilli C. Sex hormones, brain damage and clinical course of multiple sclerosis // J. Neurol. Sci.- 2009.- Vol. 286.- P. 35-39.

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Copyright (c) 2015 Abdurasulova I.N., Tarasova E.A., Ermolenko E.I., Eliseev A.V., Matsulevich A.V., Bisaga G.N., Skulyabin D.I., Suvorov A.N., Klimenko V.M.

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