Urologic Applications of the Microbiota in Multiple Sclerosis

Neurogenic Bladder (C Powell, Section Editor)
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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.

Keywords

Urological applications Microbiota Multiple sclerosis 

Notes

Compliance with Ethical Standards

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.

References

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

  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    <Analysis of gut microbiome reveals significant differences between men with CP CPPS and controls.pdf>.Google Scholar
  11. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14.CrossRefGoogle Scholar
  13. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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.PubMedPubMedCentralGoogle Scholar
  15. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Stamm WE, Norrby SR. Urinary tract infections: disease panorama and challenges. J Infect Dis. 2001;183(Suppl 1):S1–4.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedPubMedCentralGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. 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.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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.Google Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 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.PubMedCrossRefGoogle Scholar
  66. 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.PubMedCrossRefGoogle Scholar
  67. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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.PubMedCrossRefGoogle Scholar
  69. 69.
    Mahgoub M, Monteggia LM. Epigenetics and psychiatry. Neurotherapeutics. 2013;10(4):734–41.  https://doi.org/10.1007/s13311-013-0213-6.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 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.PubMedCrossRefGoogle Scholar
  71. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Thwaites R, Chamberlain G, Sacre S. Emerging role of endosomal toll-like receptors in rheumatoid arthritis. Front Immunol. 2014;5:1.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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.PubMedCrossRefGoogle Scholar
  76. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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.PubMedCrossRefGoogle Scholar
  79. 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.PubMedCrossRefGoogle Scholar
  80. 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.PubMedCrossRefGoogle Scholar
  81. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 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.PubMedCrossRefGoogle Scholar
  83. 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.PubMedCrossRefGoogle Scholar
  84. 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.PubMedCrossRefGoogle Scholar
  85. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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.PubMedCrossRefGoogle Scholar
  87. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 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.PubMedCrossRefGoogle Scholar
  89. 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.PubMedCrossRefGoogle Scholar
  90. 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.PubMedCrossRefGoogle Scholar
  91. 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.PubMedCrossRefGoogle Scholar
  92. 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.PubMedCrossRefGoogle Scholar
  93. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 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.PubMedCrossRefGoogle Scholar
  95. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 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.PubMedCrossRefGoogle Scholar
  98. 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.PubMedCrossRefGoogle Scholar
  99. 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.PubMedCrossRefGoogle Scholar
  100. 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.PubMedGoogle Scholar
  101. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 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).Google Scholar
  103. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 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.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Urology, Ochsner Medical CenterNew OrleansUSA

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