EXPLORING THE IMPACT OF GUT MICROBIOTA ON EPILEPSY PATHOGENESIS IN KRUSHINSKY-MOLODKINA RATS



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Abstract

Abstract

The gut–brain axis represents a bidirectional communication network that integrates neural, endocrine, and immune pathways with intestinal microbiota-derived signals. Disruption of this system, often resulting from gut microbiota dysbiosis, has been increasingly associated with neurological and psychiatric disorders, including depression, Alzheimer’s disease, and Parkinson’s disease. Understanding a crosstalk between host genetics, microbiota composition, and neuroinflammatory processes is therefore crucial for elucidating the mechanisms underlying brain health and disease. In the present study, we investigated gut microbiota composition in two genetically distinct rat Wistar and Krushinsky-Molodkina (KM) strains, and further assessed the effects of kindling-induced epileptogenesis and associated neuroinflammation on the KM microbiota. Our analyses revealed notable inter-group alterations in microbial composition. In particular, Enterococcus hirae abundance differed significantly between Wistar and KM control rats, while Streptococcus hyointestinalis exhibited changes between the KM control and KM kindling groups. Furthermore, we observed a reduced relative abundance of Lactobacillus murinus and Lactobacillus reuteri in KM control rats compared with both Wistar and KM kindling animals. In parallel, we observed altered expression of NF-κB p65 in the temporal lobe white matter. Specifically, Wistar vs. KM control rats displayed lower NF-κB p65 expression, whereas KM kindling rats showed reduced expression compared to the KM control group. Such alterations in NF-kB p65 expression correlate with observed shifts in abundance of Lactobacillus murinus and Lactobacillus reuteri, suggesting a link between microbiota composition and neuroinflammatory processes. These findings provide deeper insight into the multifaceted interplay between host genetic background, neuroinflammation, and gut microbial composition. The results suggest that differences in bacterial taxa, particularly within Lactobacillus species, may be linked to NF-κB–mediated processes in the brain, thereby shaping the pathophysiological landscape of neurological disorders. Further investigations are required to better understand the complex crosstalk between host genetics, brain and gut microbiota, and their implication for health and disease.

About the authors

Alim Bidzhiev

St. Petersburg Pasteur Research Institute of Epidemiology and Microbiology, St. Petersburg, Russia

Email: alimbj09@gmail.com
ORCID iD: 0009-0008-2431-4588
SPIN-code: 9815-4628

Junior Researcher at the Laboratory of Medical Bacteriology

Россия, Russia, St. Petersburg, Mira St., 14

Lyudmila Kraeva

St. Petersburg Pasteur Research Institute of Epidemiology and Microbiology, St. Petersburg, Russia;
Military Medical Academy named after S.M. Kirov" of the Ministry of Defense of the Russian Federation, St. Petersburg, Russia

Email: lykraeva@yandex.ru
ORCID iD: 0000-0002-9115-3250
SPIN-code: 4863-4001
Scopus Author ID: 23473821900
ResearcherId: H-1786-2012

Head of the Laboratory of Medical Bacteriology;

Professor of the Department of Microbiology

Россия, Russia, St. Petersburg, Mira St., 14; Saint Petersburg, Akademika Lebedeva str., 6

Andrey Ivlev

Sechenov Institute of Evolutionary Physiology and Biochemistry Russian Academy of Sciences, St. Petersburg, Russia

Email: andrewivlev1410@gmail.com
ORCID iD: 0000-0002-7182-2066
SPIN-code: 7880-9440

Junior Researcher at the Laboratory of Comparative Biochemistry of Cellular Functions

Россия, 44 Torez Ave., Saint Petersburg, Russian Federation

Alina Goncharova

St. Petersburg Pasteur Research Institute of Epidemiology and Microbiology, St. Petersburg, Russia;
Pediatric Research and Clinical Center for Infectious Diseases, St. Petersburg, Russia

Email: ar.khairullina98@gmail.com
ORCID iD: 0009-0009-6559-7892
SPIN-code: 2474-4359

Junior Researcher at the Research Department of Medical Microbiology and Molecular Epidemiology; Junior Researcher at the Laboratory of Medical Bacteriology

Россия, St. Petersburg, Professora Popova St., 9.; St. Petersburg, Mira St., 14

Elena Bazhanova

Sechenov Institute of Evolutionary Physiology and Biochemistry Russian Academy of Sciences, St. Petersburg, Russia

Author for correspondence.
Email: bazhanovae@mail.ru
ORCID iD: 0000-0002-9763-504X
SPIN-code: 1644-8113

Leading Researcher at the Laboratory of Comparative Biochemistry of Cellular Functions

Россия, 44 Torez Ave., Saint Petersburg, Russian Federation

References

  1. Бажанова Е. Д., Козлов А. А. Механизмы апоптоза при фармакорезистентной эпилепсии //НЕВРОЛОГИИ И ПСИХИАТРИИ ИМ. CC КОРСАКОВА Учредители: Общественная Организация" Всероссийское Общество Неврологов", Общественная Организация" Российское Общество Психиатров". 2022 Bazhanova ED, Kozlov AA. Mechanisms of apoptosis in drug-resistant epilepsy. Zh Nevrol Psikhiatr Im S S Korsakova. 2022;122(5):43-50. (In Russ). [[doi: 10.17116/jnevro202212205143f]
  2. Bagheri S, Heydari A, Alinaghipour A, Salami M. Effect of probiotic supplementation on seizure activity and cognitive performance in PTZ-induced chemical kindling. Epilepsy Behav. 2019 Jun;95:43-50.
  3. Bagheri S, Heydari A, Alinaghipour A, Salami M. Effect of probiotic supplementation on seizure activity and cognitive performance in PTZ-induced chemical kindling. Epilepsy Behav. 2019 Jun;95:43-50. [doi: 10.1016/j.yebeh.2019.03.038]
  4. Bercik P, Collins SM. The effects of inflammation, infection and antibiotics on the microbiota-gut-brain axis. Adv Exp Med Biol. 2014;817:279-89. Bercik P, Collins SM. The effects of inflammation, infection and antibiotics on the microbiota-gut-brain axis. Adv Exp Med Biol. 2014;817:279-89. [doi: 10.1007/978-1-4939-0897-4_13]
  5. Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol. 2014;817:373-403. Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol. 2014;817:373-403. [doi: 10.1007/978-1-4939-0897-4_17]
  6. Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, Gentile S, Belotti G, Villani D, Harach T, Bolmont T, Padovani A, Boccardi M, Frisoni GB; INDIA-FBP Group. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging. 2017 Jan;49:60-68. Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, Gentile S, Belotti G, Villani D, Harach T, Bolmont T, Padovani A, Boccardi M, Frisoni GB; INDIA-FBP Group. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging. 2017 Jan;49:60-68. [doi: 10.1016/j.neurobiolaging.2016.08.019]
  7. Chen Y, Li R, Chang Q, Dong Z, Yang H, Xu C. Lactobacillus bulgaricus or Lactobacillus rhamnosus Suppresses NF-κB Signaling Pathway and Protects against AFB₁-Induced Hepatitis: A Novel Potential Preventive Strategy for Aflatoxicosis? Toxins (Basel). 2019 Jan 4;11(1):17. Chen Y, Li R, Chang Q, Dong Z, Yang H, Xu C. Lactobacillus bulgaricus or Lactobacillus rhamnosus Suppresses NF-κB Signaling Pathway and Protects against AFB₁-Induced Hepatitis: A Novel Potential Preventive Strategy for Aflatoxicosis? Toxins (Basel). 2019 Jan 4;11(1):17. [doi: 10.3390/toxins11010017.]
  8. Fröhlich EE, Farzi A, Mayerhofer R, Reichmann F, Jačan A, Wagner B, Zinser E, Bordag N, Magnes C, Fröhlich E, Kashofer K, Gorkiewicz G, Holzer P. Cognitive impairment by antibiotic-induced gut dysbiosis: Analysis of gut microbiota-brain communication. Brain Behav Immun. 2016 Aug;56:140-55. Fröhlich EE, Farzi A, Mayerhofer R, Reichmann F, Jačan A, Wagner B, Zinser E, Bordag N, Magnes C, Fröhlich E, Kashofer K, Gorkiewicz G, Holzer P. Cognitive impairment by antibiotic-induced gut dysbiosis: Analysis of gut microbiota-brain communication. Brain Behav Immun. 2016 Aug;56:140-55. [doi: 10.1016/j.bbi.2016.02.020.f]
  9. Fung TC. The microbiota-immune axis as a central mediator of gut-brain communication. Neurobiol Dis. 2020 Mar;136:104714. Fung TC. The microbiota-immune axis as a central mediator of gut-brain communication. Neurobiol Dis. 2020 Mar;136:104714 [doi: 10.1016/j.nbd.2019.104714]
  10. Gómez-Eguílaz M, Ramón-Trapero JL, Pérez-Martínez L, Blanco JR. The beneficial effect of probiotics as a supplementary treatment in drug-resistant epilepsy: a pilot study. Benef Microbes. 2018 Dec 7;9(6):875-881. Gómez-Eguílaz M, Ramón-Trapero JL, Pérez-Martínez L, Blanco JR. The beneficial effect of probiotics as a supplementary treatment in drug-resistant epilepsy: a pilot study. Benef Microbes. 2018 Dec 7;9(6):875-881. [doi: 10.3920/BM2018.0018]
  11. Hofer U. Microbiome: pro-inflammatory Prevotella? Nat Rev Microbiol. 2014 Jan;12(1):5. Hofer U. Microbiome: pro-inflammatory Prevotella? Nat Rev Microbiol. 2014 Jan;12(1):5. [doi: 10.1038/nrmicro3180]
  12. Houser MC, Tansey MG. The gut-brain axis: is intestinal inflammation a silent driver of Parkinson's disease pathogenesis? NPJ Parkinsons Dis. 2017 Jan 11;3:3. Houser MC, Tansey MG. The gut-brain axis: is intestinal inflammation a silent driver of Parkinson's disease pathogenesis? NPJ Parkinsons Dis. 2017 Jan 11;3:3. [doi: 10.1038/s41531-016-0002-0]
  13. Khan I, Ullah N, Zha L, Bai Y, Khan A, Zhao T, Che T, Zhang C. Alteration of Gut Microbiota in Inflammatory Bowel Disease (IBD): Cause or Consequence? IBD Treatment Targeting the Gut Microbiome. Pathogens. 2019 Aug 13;8(3):126. Khan I, Ullah N, Zha L, Bai Y, Khan A, Zhao T, Che T, Zhang C. Alteration of Gut Microbiota in Inflammatory Bowel Disease (IBD): Cause or Consequence? IBD Treatment Targeting the Gut Microbiome. Pathogens. 2019 Aug 13;8(3):126. [doi: 10.3390/pathogens8030126]
  14. Kim SL, Choi HS, Ko YC, Yun BS, Lee DS. 5-Hydroxymaltol Derived from Beetroot Juice through Lactobacillus Fermentation Suppresses Inflammatory Effect and Oxidant Stress via Regulating NF-kB, MAPKs Pathway and NRF2/HO-1 Expression. Antioxidants (Basel). 2021 Aug 23;10(8):1324. Kim SL, Choi HS, Ko YC, Yun BS, Lee DS. 5-Hydroxymaltol Derived from Beetroot Juice through Lactobacillus Fermentation Suppresses Inflammatory Effect and Oxidant Stress via Regulating NF-kB, MAPKs Pathway and NRF2/HO-1 Expression. Antioxidants (Basel). 2021 Aug 23;10(8):1324. [doi: 10.3390/antiox10081324]
  15. Kong L, Chen J, Ji X, Qin Q, Yang H, Liu D, Li D, Sun M. Alcoholic fatty liver disease inhibited the co-expression of Fmo5 and PPARα to activate the NF-κB signaling pathway, thereby reducing liver injury via inducing gut microbiota disturbance. J Exp Clin Cancer Res. 2021 Jan 7;40(1):18. Kong L, Chen J, Ji X, Qin Q, Yang H, Liu D, Li D, Sun M. Alcoholic fatty liver disease inhibited the co-expression of Fmo5 and PPARα to activate the NF-κB signaling pathway, thereby reducing liver injury via inducing gut microbiota disturbance. J Exp Clin Cancer Res. 2021 Jan 7;40(1):18. [doi: 10.1186/s13046-020-01782-w ]
  16. Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, Tajabadi-Ebrahimi M, Jafari P, Asemi Z. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin Nutr. 2017 Oct;36(5):1245-1249. Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, Tajabadi-Ebrahimi M, Jafari P, Asemi Z. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin Nutr. 2017 Oct;36(5):1245-1249 [doi: 10.1016/j.clnu.2016.08.015 ]
  17. Li H, Wang Y, Zhao C, Liu J, Zhang L, Li A. Fecal transplantation can alleviate tic severity in a Tourette syndrome mouse model by modulating intestinal flora and promoting serotonin secretion. Chin Med J (Engl). 2022 Mar 20;135(6):707-713. Li H, Wang Y, Zhao C, Liu J, Zhang L, Li A. Fecal transplantation can alleviate tic severity in a Tourette syndrome mouse model by modulating intestinal flora and promoting serotonin secretion. Chin Med J (Engl). 2022 Mar 20;135(6):707-713. [doi: 10.1097/CM9.0000000000001885 4]
  18. Liu L, Huh JR, Shah K. Microbiota and the gut-brain-axis: Implications for new therapeutic design in the CNS. EBioMedicine. 2022 Mar;77:103908. Liu L, Huh JR, Shah K. Microbiota and the gut-brain-axis: Implications for new therapeutic design in the CNS. EBioMedicine. 2022 Mar;77:103908. [doi: 10.1016/j.ebiom.2022.103908]
  19. Mao J, Qi S, Cui Y, Dou X, Luo XM, Liu J, Zhu T, Ma Y, Wang H. Lactobacillus rhamnosus GG Attenuates Lipopolysaccharide-Induced Inflammation and Barrier Dysfunction by Regulating MAPK/NF-κB Signaling and Modulating Metabolome in the Piglet Intestine. J Nutr. 2020 May 1;150(5):1313-1323. Mao J, Qi S, Cui Y, Dou X, Luo XM, Liu J, Zhu T, Ma Y, Wang H. Lactobacillus rhamnosus GG Attenuates Lipopolysaccharide-Induced Inflammation and Barrier Dysfunction by Regulating MAPK/NF-κB Signaling and Modulating Metabolome in the Piglet Intestine. J Nutr. 2020 May 1;150(5):1313-1323. [doi: 10.1093/jn/nxaa009 ]
  20. Moradi K, Ashraf-Ganjouei A, Tavolinejad H, Bagheri S, Akhondzadeh S. The interplay between gut microbiota and autism spectrum disorders: A focus on immunological pathways. Prog Neuropsychopharmacol Biol Psychiatry. 2021 Mar 2;106:110091. Moradi K, Ashraf-Ganjouei A, Tavolinejad H, Bagheri S, Akhondzadeh S. The interplay between gut microbiota and autism spectrum disorders: A focus on immunological pathways. Prog Neuropsychopharmacol Biol Psychiatry. 2021 Mar 2;106:110091. [doi: 10.1016/j.pnpbp.2020.11009]
  21. Peng A, Qiu X, Lai W, Li W, Zhang L, Zhu X, He S, Duan J, Chen L. Altered composition of the gut microbiome in patients with drug-resistant epilepsy. Epilepsy Res. 2018 Nov;147:102-107. Peng A, Qiu X, Lai W, Li W, Zhang L, Zhu X, He S, Duan J, Chen L. Altered composition of the gut microbiome in patients with drug-resistant epilepsy. Epilepsy Res. 2018 Nov;147:102-107. [doi: 10.1016/j.eplepsyres.2018.09.013]
  22. Qiu X, Zhang M, Yang X, Hong N, Yu C. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J Crohns Colitis. 2013 Dec;7(11):e558-68. Qiu X, Zhang M, Yang X, Hong N, Yu C. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J Crohns Colitis. 2013 Dec;7(11):e558-68. [doi: 10.1016/j.crohns.2013.04.002]
  23. Romijn JA, Corssmit EP, Havekes LM, Pijl H. Gut-brain axis. Curr Opin Clin Nutr Metab Care. 2008 Jul;11(4):518-21. Romijn JA, Corssmit EP, Havekes LM, Pijl H. Gut-brain axis. Curr Opin Clin Nutr Metab Care. 2008 Jul;11(4):518-21. [doi: 10.1097/MCO.0b013e328302c9b0 f]
  24. Rothhammer V, Borucki DM, Tjon EC, Takenaka MC, Chao CC, Ardura-Fabregat A, de Lima KA, Gutiérrez-Vázquez C, Hewson P, Staszewski O, Blain M, Healy L, Neziraj T, Borio M, Wheeler M, Dragin LL, Laplaud DA, Antel J, Alvarez JI, Prinz M, Quintana FJ. Microglial control of astrocytes in response to microbial metabolites. Nature. 2018 May;557(7707):724-728. Rothhammer V, Borucki DM, Tjon EC, Takenaka MC, Chao CC, Ardura-Fabregat A, de Lima KA, Gutiérrez-Vázquez C, Hewson P, Staszewski O, Blain M, Healy L, Neziraj T, Borio M, Wheeler M, Dragin LL, Laplaud DA, Antel J, Alvarez JI, Prinz M, Quintana FJ. Microglial control of astrocytes in response to microbial metabolites. Nature. 2018 May;557(7707):724-728. [doi: 10.1038/s41586-018-0119-xf]
  25. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12204-9. doi: 10.1073/pnas.0909122107 Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12204-9. doi: 10.1073/pnas.0909122107 [doi: 10.1073/pnas.09091221071]
  26. Rutsch A, Kantsjö JB, Ronchi F. The Gut-Brain Axis: How Microbiota and Host Inflammasome Influence Brain Physiology and Pathology. Front Immunol. 2020 Dec 10;11:604179. Rutsch A, Kantsjö JB, Ronchi F. The Gut-Brain Axis: How Microbiota and Host Inflammasome Influence Brain Physiology and Pathology. Front Immunol. 2020 Dec 10;11:604179. [doi: 10.3389/fimmu.2020.604179 ]
  27. Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M, Franzosa EA, Ter Horst R, Jansen T, Jacobs L, Bonder MJ, Kurilshikov A, Fu J, Joosten LAB, Zhernakova A, Huttenhower C, Wijmenga C, Netea MG, Xavier RJ. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell. 2016 Nov 3;167(4):1125-1136.e8. Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M, Franzosa EA, Ter Horst R, Jansen T, Jacobs L, Bonder MJ, Kurilshikov A, Fu J, Joosten LAB, Zhernakova A, Huttenhower C, Wijmenga C, Netea MG, Xavier RJ. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell. 2016 Nov 3;167(4):1125-1136.e8. [doi: 10.1016/j.cell.2016.10.020]
  28. Secher T, Kassem S, Benamar M, Bernard I, Boury M, Barreau F, Oswald E, Saoudi A. 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 Sep 14;8:1096. Secher T, Kassem S, Benamar M, Bernard I, Boury M, Barreau F, Oswald E, Saoudi A. 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 Sep 14;8:1096. [doi: 10.3389/fimmu.2017.01096]
  29. Serra D, Almeida LM, Dinis TCP. The Impact of Chronic Intestinal Inflammation on Brain Disorders: the Microbiota-Gut-Brain Axis. Mol Neurobiol. 2019 Oct;56(10):6941-6951. Serra D, Almeida LM, Dinis TCP. The Impact of Chronic Intestinal Inflammation on Brain Disorders: the Microbiota-Gut-Brain Axis. Mol Neurobiol. 2019 Oct;56(10):6941-6951. [doi: 10.1007/s12035-019-1572-8]
  30. Sundman MH, Chen NK, Subbian V, Chou YH. The bidirectional gut-brain-microbiota axis as a potential nexus between traumatic brain injury, inflammation, and disease. Brain Behav Immun. 2017 Nov;66:31-44. Sundman MH, Chen NK, Subbian V, Chou YH. The bidirectional gut-brain-microbiota axis as a potential nexus between traumatic brain injury, inflammation, and disease. Brain Behav Immun. 2017 Nov;66:31-44. [doi: 10.1016/j.bbi.2017.05.009 ]
  31. Surina NM, Fedotova IB, Nikolaev GM, Grechenko VV, Gankovskaya LV, Ogurtsova AD, Poletaeva II. Neuroinflammation in Pathogenesis of Audiogenic Epilepsy: Altered Proinflammatory Cytokine Levels in the Rats of Krushinsky-Molodkina Seizure-Prone Strain. Biochemistry (Mosc). 2023 Apr;88(4):481-490. doi: 10.1134/S0006297923040041 Surina NM, Fedotova IB, Nikolaev GM, Grechenko VV, Gankovskaya LV, Ogurtsova AD, Poletaeva II. Neuroinflammation in Pathogenesis of Audiogenic Epilepsy: Altered Proinflammatory Cytokine Levels in the Rats of Krushinsky-Molodkina Seizure-Prone Strain. Biochemistry (Mosc). 2023 Apr;88(4):481-490. doi: 10.1134/S0006297923040041 [doi: 10.1134/S0006297923040041r]
  32. Tankou SK, Regev K, Healy BC, Cox LM, Tjon E, Kivisakk P, Vanande IP, Cook S, Gandhi R, Glanz B, Stankiewicz J, Weiner HL. Investigation of probiotics in multiple sclerosis. Mult Scler. 2018 Jan;24(1):58-63. Tankou SK, Regev K, Healy BC, Cox LM, Tjon E, Kivisakk P, Vanande IP, Cook S, Gandhi R, Glanz B, Stankiewicz J, Weiner HL. Investigation of probiotics in multiple sclerosis. Mult Scler. 2018 Jan;24(1):58-63. [doi: 10.1177/1352458517737390]
  33. Vos P, Garrity G, Jones D, Krieg N R, Ludwig W, Rainey F A, Schleifer K, Whitman WB. Bergey's Manual of Systematic Bacteriology: Volume 3: The Firmicutes. Springer New York, NY; 2009. p. 464 – 513. Vos P, Garrity G, Jones D, Krieg N R, Ludwig W, Rainey F A, Schleifer K, Whitman WB. Bergey's Manual of Systematic Bacteriology: Volume 3: The Firmicutes. Springer New York, NY; 2009. p. 464 – 513. [https://www.researchgate.net/profile/Alaa_Niamah/post/Lactobacillus_casei_is_the_same_that_Lactobacillus_paracasei/attachment/59d64f0779197b80779a8480/AS%3A495670448869376%401495188452895/download/bergey%27s+manual+of+systematic+bacteriology+2009.pdff]

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