Skip to main content

Advertisement

SpringerLink
Log in

Urologic Applications of the Microbiota in Multiple Sclerosis

  • Neurogenic Bladder (C Powell, Section Editor)
  • Published:
Current Bladder Dysfunction Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

In this review, we report on the factors conferring a healthy microbiome, applications in the urinary tract with urgency, urge incontinence, and urinary tract infection and interactions of the Gut-Brain Axis as they apply to multiple sclerosis. Clinical applications in the use of probiotics are briefly reviewed.

Recent Findings

Information from the Human Microbiome Project has spurred exponential studies which have opened up exciting possibilities in many fields. Of particular interest is how these concepts apply to the study of microbes in the urinary tract, vagina, and intestines and how they interact not only with each other but also the brain.

Summary

The ways that microbes affect the lower urinary tract as well as overall wellbeing are currently being explored.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, et al. The sequence of the human genome. Science. 2001;291(5507):1304–51. https://doi.org/10.1126/science.1058040.

    Article  PubMed  CAS  Google Scholar 

  2. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human micobiome project. Nature. 2007;449(7164):804–10. https://doi.org/10.1038/nature06244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. •• Nickel JC, Stephens A, Landis JR, Mullins C, van Bokhoven A, Lucia MS, et al. Assessment of the lower urinary tract microbiota during symptom flare in women with urologic chronic pelvic pain syndrome: A MAPP Network Study. J Urol. 2016;195(2):356–62. Study with significant clinical implications for IC patients.

    Article  PubMed  Google Scholar 

  4. Jacquemin J, Ammiraju JS, Haberer G, Billheimer DD, Yu Y, Liu LC, et al. Fifteen million years of evolution in the Oryza genus shows extensive gene family expansion. Mol Plant. 2014;7(4):642–56. https://doi.org/10.1093/mp/sst149.

    Article  PubMed  CAS  Google Scholar 

  5. Brookfield JF. Genomic sequencing: the complexity conundrum. Curr Biol. 2000;10(14):R514–5. https://doi.org/10.1016/S0960-9822(00)00581-9.

    Article  PubMed  CAS  Google Scholar 

  6. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–9. https://doi.org/10.1126/science.1124234.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Thomas-White K, Brady M, Wolfe AJ, Mueller ER. The bladder is not sterile: history and current discoveries on the urinary microbiome. Curr Bladder Dysfunct Rep. 2016;11(1):18–24. https://doi.org/10.1007/s11884-016-0345-8.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Integrative HMPRNC. The integrative human microbiome project: dynamic analysis of microbiome-host omics profiles during periods of human health and disease. Cell Host Microbe. 2014;16(3):276–89.

    Article  Google Scholar 

  9. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature. 2014;509(7500):357–60. https://doi.org/10.1038/nature13178.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. <Analysis of gut microbiome reveals significant differences between men with CP CPPS and controls.pdf>.

  11. • Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med. 2016;8(1):51. Excellent review of a healthy human microbiome.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14.

    Article  Google Scholar 

  13. Shafquat A, Joice R, Simmons SL, Huttenhower C. Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol. 2014;22(5):261–6. https://doi.org/10.1016/j.tim.2014.01.011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–7. https://doi.org/10.1038/nature11053.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107(33):14691–6. https://doi.org/10.1073/pnas.1005963107.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Takeshita T, Matsuo K, Furuta M, Shibata Y, Fukami K, Shimazaki Y, et al. Distinct composition of the oral indigenous microbiota in South Korean and Japanese adults. Sci Rep. 2014;4:6990.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Tyakht AV, Kostryukova ES, Popenko AS, Belenikin MS, Pavlenko AV, Larin AK, et al. Human gut microbiota community structures in urban and rural populations in Russia. Nat Commun. 2013;4:2469.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhang J, Guo Z, Xue Z, Sun Z, Zhang M, Wang L, et al. A phylo-functional core of gut microbiota in healthy young Chinese cohorts across lifestyles, geography and ethnicities. ISME J. 2015;9(9):1979–90. https://doi.org/10.1038/ismej.2015.11.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Duranti S, Lugli GA, Mancabelli L, Armanini F, Turroni F, James K, et al. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome. 2017;5(1):66. https://doi.org/10.1186/s40168-017-0282-6.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra65. https://doi.org/10.1126/scitranslmed.3008599.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016;16(1):86. https://doi.org/10.1186/s12876-016-0498-0.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Okada H, Kuhn C, Feillet H, Bach JF. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010;160(1):1–9. https://doi.org/10.1111/j.1365-2249.2010.04139.x.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332(6032):974–7. https://doi.org/10.1126/science.1206095.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Begum-Haque S, Dasgupta S, et al. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J Immunol. 2010;185(7):4101–8. https://doi.org/10.4049/jimmunol.1001443.

    Article  PubMed  CAS  Google Scholar 

  25. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science. 2012;336(6086):1255–62. https://doi.org/10.1126/science.1224203.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T. Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci U S A. 2011;108(34):14288–93. https://doi.org/10.1073/pnas.1101591108.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Flores GE, Caporaso JG, Henley JB, Rideout JR, Domogala D, Chase J, et al. Temporal variability is a personalized feature of the human microbiome. Genome Biol. 2014;15(12):531. https://doi.org/10.1186/s13059-014-0531-y.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Hartstra AV, Bouter KE, Backhed F, Nieuwdorp M. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care. 2015;38(1):159–65. https://doi.org/10.2337/dc14-0769.

    Article  PubMed  CAS  Google Scholar 

  29. Kim D, Zeng MY, Nunez G. The interplay between host immune cells and gut microbiota in chronic inflammatory diseases. Exp Mol Med. 2017;49(5):e339. https://doi.org/10.1038/emm.2017.24.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. van Tongeren SP, Slaets JP, Harmsen HJ, Welling GW. Fecal microbiota composition and frailty. Appl Environ Microbiol. 2005;71(10):6438–42. https://doi.org/10.1128/AEM.71.10.6438-6442.2005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16(7):1024–33. https://doi.org/10.1111/cmi.12308.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Cabrera-Perez J, Badovinac VP, Griffith TS. Enteric immunity, the gut microbiome, and sepsis: rethinking the germ theory of disease. Exp Biol Med (Maywood). 2017;242(2):127–39. https://doi.org/10.1177/1535370216669610.

    Article  CAS  Google Scholar 

  33. • Brubaker L, Wolfe AJ. The female urinary microbiota, urinary health and common urinary disorders. Ann Transl Med. 2017;5(2):34. https://doi.org/10.21037/atm.2016.11.62. Important work recognizing that urine is not sterile.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Siddiqui H, Nederbragt AJ, Lagesen K, Jeansson SL, Jakobsen KS. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol. 2011;11(1):244. https://doi.org/10.1186/1471-2180-11-244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Khasriya R, Sathiananthamoorthy S, Ismail S, Kelsey M, Wilson M, Rohn JL, et al. Spectrum of bacterial colonization associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol. 2013;51(7):2054–62. https://doi.org/10.1128/JCM.03314-12.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Bao Y, Al KF, Chanyi RM, Whiteside S, Dewar M, Razvi H, et al. Questions and challenges associated with studying the microbiome of the urinary tract. Ann Transl Med. 2017;5(2):33. https://doi.org/10.21037/atm.2016.12.14.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Whiteside SA, Razvi H, Dave S, Reid G, Burton JP. The microbiome of the urinary tract—a role beyond infection. Nat Rev Urol. 2015;12(2):81–90. https://doi.org/10.1038/nrurol.2014.361.

    Article  PubMed  Google Scholar 

  38. Wolfe AJ, Brubaker L. “Sterile urine” and the presence of bacteria. Eur Urol. 2015;68(2):173–4. https://doi.org/10.1016/j.eururo.2015.02.041.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ackerman AL, Underhill DM. The mycobiome of the human urinary tract: potential roles for fungi in urology. Ann Transl Med. 2017;5(2):31. https://doi.org/10.21037/atm.2016.12.69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Dollive S, Peterfreund GL, Sherrill-Mix S, Bittinger K, Sinha R, Hoffmann C, et al. A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol. 2012;13(7):R60. https://doi.org/10.1186/gb-2012-13-7-r60.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med. 2007;4(12):e329. https://doi.org/10.1371/journal.pmed.0040329.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K, Fok C, et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. MBio. 2014;5(4):e01283–14. https://doi.org/10.1128/mBio.01283-14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Brubaker L, Nager CW, Richter HE, Visco A, Nygaard I, Barber MD, et al. Urinary bacteria in adult women with urgency urinary incontinence. Int Urogynecol J. 2014;25(9):1179–84. https://doi.org/10.1007/s00192-013-2325-2.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Stamm WE, Norrby SR. Urinary tract infections: disease panorama and challenges. J Infect Dis. 2001;183(Suppl 1):S1–4.

    Article  PubMed  Google Scholar 

  45. Murray BE, Rensimer ER, DuPont HL. Emergence of high-level trimethoprim resistance in fecal Escherichia coli during oral administration of trimethoprim or trimethoprim—sulfamethoxazole. N Engl J Med. 1982;306(3):130–5. https://doi.org/10.1056/NEJM198201213060302.

    Article  PubMed  CAS  Google Scholar 

  46. Chan RC, Reid G, Irvin RT, Bruce AW, Costerton JW. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985;47(1):84–9.

    PubMed  PubMed Central  CAS  Google Scholar 

  47. Baerheim A, Larsen E, Digranes A. Vaginal application of lactobacilli in the prophylaxis of recurrent lower urinary tract infection in women. Scand J Prim Health Care. 1994;12(4):239–43. https://doi.org/10.3109/02813439409029247.

    Article  PubMed  CAS  Google Scholar 

  48. Kontiokari T, Sundqvist K, Nuutinen M, Pokka T, Koskela M, Uhari M. Randomised trial of cranberry-lingonberry juice and Lactobacillus GG drink for the prevention of urinary tract infections in women. BMJ. 2001;322(7302):1571. https://doi.org/10.1136/bmj.322.7302.1571.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Stapleton AE, Au-Yeung M, Hooton TM, Fredricks DN, Roberts PL, Czaja CA, et al. Randomized, placebo-controlled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin Infect Dis. 2011;52(10):1212–7. https://doi.org/10.1093/cid/cir183.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Beerepoot MA, ter Riet G, Nys S, van der Wal WM, de Borgie CA, de Reijke TM, et al. Lactobacilli vs antibiotics to prevent urinary tract infections: a randomized, double-blind, noninferiority trial in postmenopausal women. Arch Intern Med. 2012;172(9):704–12. https://doi.org/10.1001/archinternmed.2012.777.

    Article  PubMed  CAS  Google Scholar 

  51. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269–84. https://doi.org/10.1038/nrmicro3432.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Hull R, Rudy D, Donovan W, Svanborg C, Wieser I, Stewart C, et al. Urinary tract infection prophylaxis using Escherichia coli 83972 in spinal cord injured patients. J Urol. 2000;163(3):872–7. https://doi.org/10.1016/S0022-5347(05)67823-8.

    Article  PubMed  CAS  Google Scholar 

  53. Singh R, van Nood E, Nieuwdorp M, van Dam B, ten Berge IJ, Geerlings SE, et al. Donor feces infusion for eradication of extended spectrum beta-lactamase producing Escherichia coli in a patient with end stage renal disease. Clin Microbiol Infect. 2014;20(11):O977–8. https://doi.org/10.1111/1469-0691.12683.

    Article  PubMed  CAS  Google Scholar 

  54. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part II: noninfectious factors. Ann Neurol. 2007;61(6):504–13. https://doi.org/10.1002/ana.21141.

    Article  PubMed  CAS  Google Scholar 

  55. Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol. 2007;61(4):288–99. https://doi.org/10.1002/ana.21117.

    Article  PubMed  Google Scholar 

  56. • Galland L. The gut microbiome and the brain. J Med Food. 2014;17(12):1261–72. https://doi.org/10.1089/jmf.2014.7000. Excellent comprehensive review of the the Gut/CNS axis.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. • Fleck AK, Schuppan D, Wiendl H, Klotz L. Gut-CNS-axis as possibility to modulate inflammatory disease activity-implications for multiple sclerosis. Int J Mol Sci. 2017;18(7). The latest review with regards to the GUT/CNS axis and MS.

  58. Reigstad CS, Salmonson CE, Rainey JF 3rd, Szurszewski JH, Linden DR, Sonnenburg JL, et al. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J. 2015;29(4):1395–403. https://doi.org/10.1096/fj.14-259598.

    Article  PubMed  CAS  Google Scholar 

  59. Weinstein LI, Revuelta A, Pando RH. Catecholamines and acetylcholine are key regulators of the interaction between microbes and the immune system. Ann N Y Acad Sci. 2015;1351(1):39–51. https://doi.org/10.1111/nyas.12792.

    Article  PubMed  CAS  Google Scholar 

  60. Stephenson M, Rowatt E. The production of acetylcholine by a strain of Lactobacillus plantarum. J Gen Microbiol. 1947;1(3):279–98. https://doi.org/10.1099/00221287-1-3-279.

    Article  PubMed  CAS  Google Scholar 

  61. Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M, Taketani M, et al. Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe. 2014;16(4):495–503. https://doi.org/10.1016/j.chom.2014.09.001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Asano Y, Hiramoto T, Nishino R, Aiba Y, Kimura T, Yoshihara K, et al. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol. 2012;303(11):G1288–95. https://doi.org/10.1152/ajpgi.00341.2012.

    Article  PubMed  CAS  Google Scholar 

  63. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108(38):16050–5. https://doi.org/10.1073/pnas.1102999108.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C. Gamma-aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113(2):411–7. https://doi.org/10.1111/j.1365-2672.2012.05344.x.

    Article  PubMed  CAS  Google Scholar 

  65. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006;40(3):235–43. https://doi.org/10.1097/00004836-200603000-00015.

    Article  PubMed  CAS  Google Scholar 

  66. De Preter V, Geboes KP, Bulteel V, Vandermeulen G, Suenaert P, Rutgeerts P, et al. Kinetics of butyrate metabolism in the normal colon and in ulcerative colitis: the effects of substrate concentration and carnitine on the beta-oxidation pathway. Aliment Pharmacol Ther. 2011;34(5):526–32. https://doi.org/10.1111/j.1365-2036.2011.04757.x.

    Article  PubMed  Google Scholar 

  67. Segain JP, Raingeard, de la Bletiere D, Bourreille A, Leray V, Gervois N, et al. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut. 2000;47(3):397–403. https://doi.org/10.1136/gut.47.3.397.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Harrison IF, Dexter DT. Epigenetic targeting of histone deacetylase: therapeutic potential in Parkinson’s disease? Pharmacol Ther. 2013;140(1):34–52. https://doi.org/10.1016/j.pharmthera.2013.05.010.

    Article  PubMed  CAS  Google Scholar 

  69. Mahgoub M, Monteggia LM. Epigenetics and psychiatry. Neurotherapeutics. 2013;10(4):734–41. https://doi.org/10.1007/s13311-013-0213-6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Graff J, Tsai LH. The potential of HDAC inhibitors as cognitive enhancers. Annu Rev Pharmacol Toxicol. 2013;53(1):311–30. https://doi.org/10.1146/annurev-pharmtox-011112-140216.

    Article  PubMed  CAS  Google Scholar 

  71. Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, et al. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil. 2013;25(9):733–e575. https://doi.org/10.1111/nmo.12153.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H, Ferrier L, et al. Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology. 2012;37(11):1885–95. https://doi.org/10.1016/j.psyneuen.2012.03.024.

    Article  PubMed  CAS  Google Scholar 

  73. Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci. 2006;8(4):383–95.

    PubMed  PubMed Central  Google Scholar 

  74. Thwaites R, Chamberlain G, Sacre S. Emerging role of endosomal toll-like receptors in rheumatoid arthritis. Front Immunol. 2014;5:1.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2011;25(3):397–407. https://doi.org/10.1016/j.bbi.2010.10.023.

    Article  PubMed  CAS  Google Scholar 

  76. Silverman MN, Sternberg EM. Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann N Y Acad Sci. 2012;1261(1):55–63. https://doi.org/10.1111/j.1749-6632.2012.06633.x.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Yokote H, Miyake S, Croxford JL, 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;173(6):1714–23. https://doi.org/10.2353/ajpath.2008.080622.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Foureau DM, Haque-Begum S, et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol. 2009;183(10):6041–50. https://doi.org/10.4049/jimmunol.0900747.

    Article  PubMed  CAS  Google Scholar 

  79. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature. 2011;479(7374):538–41. https://doi.org/10.1038/nature10554.

    Article  PubMed  CAS  Google Scholar 

  80. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4615–22. https://doi.org/10.1073/pnas.1000082107.

    Article  PubMed  Google Scholar 

  81. 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):e9009. https://doi.org/10.1371/journal.pone.0009009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Yacyshyn B, Meddings J, Sadowski D, Bowen-Yacyshyn MB. Multiple sclerosis patients have peripheral blood CD45RO+ B cells and increased intestinal permeability. Dig Dis Sci. 1996;41(12):2493–8. https://doi.org/10.1007/BF02100148.

    Article  PubMed  CAS  Google Scholar 

  83. Buscarinu MC, Cerasoli B, Annibali V, Policano C, Lionetto L, Capi M, et al. Altered intestinal permeability in patients with relapsing-remitting multiple sclerosis: a pilot study. Mult Scler. 2017;23(3):442–6. https://doi.org/10.1177/1352458516652498.

    Article  PubMed  Google Scholar 

  84. Bengmark S. Gut microbial ecology in critical illness: is there a role for prebiotics, probiotics, and synbiotics? Curr Opin Crit Care. 2002;8(2):145–51. https://doi.org/10.1097/00075198-200204000-00010.

    Article  PubMed  Google Scholar 

  85. Patel R, DuPont HL. New approaches for bacteriotherapy: prebiotics, new-generation probiotics, and synbiotics. Clin Infect Dis. 2015;60(Suppl 2):S108–21. https://doi.org/10.1093/cid/civ177.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Flynn S, van Sinderen D, Thornton GM, Holo H, Nes IF, Collins JK. Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology. 2002;148(Pt 4):973–84. https://doi.org/10.1099/00221287-148-4-973.

    Article  PubMed  CAS  Google Scholar 

  87. Asahara T, Shimizu K, Nomoto K, Hamabata T, Ozawa A, Takeda Y. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157:H7. Infect Immun. 2004;72(4):2240–7. https://doi.org/10.1128/IAI.72.4.2240-2247.2004.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Grosse C, Scherer J, Koch D, Otto M, Taudte N, Grass G. A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol. 2006;62(1):120–31. https://doi.org/10.1111/j.1365-2958.2006.05326.x.

    Article  PubMed  CAS  Google Scholar 

  89. Sakaguchi T, Kohler H, Gu X, McCormick BA, Reinecker HC. Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells. Cell Microbiol. 2002;4(6):367–81. https://doi.org/10.1046/j.1462-5822.2002.00197.x.

    Article  PubMed  CAS  Google Scholar 

  90. Wyatt J, Vogelsang H, Hubl W, Waldhoer T, Lochs H. Intestinal permeability and the prediction of relapse in Crohn’s disease. Lancet. 1993;341(8858):1437–9. https://doi.org/10.1016/0140-6736(93)90882-H.

    Article  PubMed  CAS  Google Scholar 

  91. Schmitz H, Barmeyer C, Fromm M, Runkel N, Foss HD, Bentzel CJ, et al. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology. 1999;116(2):301–9. https://doi.org/10.1016/S0016-5085(99)70126-5.

    Article  PubMed  CAS  Google Scholar 

  92. Zhang Z, Hinrichs DJ, Lu H, Chen H, Zhong W, Kolls JK. After interleukin-12p40, are interleukin-23 and interleukin-17 the next therapeutic targets for inflammatory bowel disease? Int Immunopharmacol. 2007;7(4):409–16. https://doi.org/10.1016/j.intimp.2006.09.024.

    Article  PubMed  CAS  Google Scholar 

  93. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem. 2002;277(52):50959–65. https://doi.org/10.1074/jbc.M207050200.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res. 1992;32(2):141–4. https://doi.org/10.1203/00006450-199208000-00002.

    Article  PubMed  CAS  Google Scholar 

  95. • Doron S, Snydman DR. Risk and safety of probiotics. Clin Infect Dis. 2015;60(Suppl 2):S129–34. Nice review of the safety of probiotics.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Ebner S, Smug LN, Kneifel W, Salminen SJ, Sanders ME. Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol. 2014;20(43):16095–100. https://doi.org/10.3748/wjg.v20.i43.16095.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Salminen MK, Tynkkynen S, Rautelin H, Saxelin M, Vaara M, Ruutu P, et al. Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis. 2002;35(10):1155–60. https://doi.org/10.1086/342912.

    Article  PubMed  Google Scholar 

  98. Rayes N, Seehofer D, Hansen S, Boucsein K, Muller AR, Serke S, et al. Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation. 2002;74(1):123–7. https://doi.org/10.1097/00007890-200207150-00021.

    Article  PubMed  Google Scholar 

  99. Rayes N, Seehofer D, Theruvath T, Schiller RA, Langrehr JM, Jonas S, et al. Supply of pre- and probiotics reduces bacterial infection rates after liver transplantation—a randomized, double-blind trial. Am J Transplant. 2005;5(1):125–30. https://doi.org/10.1111/j.1600-6143.2004.00649.x.

    Article  PubMed  Google Scholar 

  100. Anukam KC, Osazuwa EO, Osadolor HB, Bruce AW, Reid G. Yogurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhea and increases CD4 count in HIV/AIDS patients. J Clin Gastroenterol. 2008;42(3):239–43. https://doi.org/10.1097/MCG.0b013e31802c7465.

    Article  PubMed  Google Scholar 

  101. Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z, Wang B, et al. The microbiome of uncontacted Amerindians. Sci Adv. 2015;1(3).

  103. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hormannsperger G, et al. Safety assessment of probiotics for human use. Gut Microbes. 2010;1(3):164–85. https://doi.org/10.4161/gmic.1.3.12127.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Donovan SM, Schneeman B, Gibson GR, Sanders ME. Establishing and evaluating health claims for probiotics. Adv Nutr. 2012;3(5):723–5. https://doi.org/10.3945/an.112.002592.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Urology, Ochsner Medical Center, New Orleans, LA, USA

    Danica May & Joanna M. Togami

Authors
  1. Danica May
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanna M. Togami
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joanna M. Togami.

Ethics declarations

Conflict of Interest

Dr. May has nothing to disclose.

Dr. Togami received research funds from Astellas and Medtronic.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Neurogenic Bladder

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

May, D., Togami, J.M. Urologic Applications of the Microbiota in Multiple Sclerosis. Curr Bladder Dysfunct Rep 13, 66–74 (2018). https://doi.org/10.1007/s11884-018-0461-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11884-018-0461-8

Keywords

Search

Navigation