European Journal of Pediatrics

, Volume 168, Issue 3, pp 253–265

Saccharomyces boulardii in childhood

Review

Abstract

Introduction

Probiotics are live microorganisms which confer a health benefit on the host. Saccharomyces boulardii, a yeast, has been found to be an effective probiotic in double-blind placebo-controlled randomized clinical studies.

Materials and methods

We reviewed the established mechanisms of actions and clinical efficacy in children of S. boulardii.

Conclusions

The mechanisms of action of S. boulardii depend mainly on the inhibition of some bacterial toxins, anti-inflammatory effects, and on stimulating effects on the intestinal mucosa such as trophic effects on the brush border enzymes and immunostimulatory effects. At present, in pediatric populations, there is evidence that S. boulardii is beneficial for the treatment of acute gastroenteritis and the prevention of antibiotic-associated diarrhea. More data are needed in other indications such as traveller’s diarrhea, Helicobacter pylori eradication, and inflammatory bowel disease. S. boulardii is a yeast strain that has been extensively studied in vitro and in vivo. Recent data have opened the door for new therapeutic indications.

Keywords

Child Diarrhea Gastroenteritis Probiotic Saccharomyces boulardii Yeast 

References

  1. 1.
    Andersson H, Asp NG, Bruce A et al (2001) Health effects of probiotics and prebiotics. A literature review on human studies. Scand J Nutr 45:58–95Google Scholar
  2. 2.
    Barbut F, Meynard JL, Guiguet M et al (1997) Clostridium difficile-associated diarrhea in HIV infected patients: epidemiology and risk factors. J Acq Immun Def Synd 16:176–181Google Scholar
  3. 3.
    Bartlett JG, Chang TW, Gurwith M et al (1978) Antibiotic-associated pseudomembranous colitis due to toxin producing Clostridia. N Engl J Med 298:531–534PubMedGoogle Scholar
  4. 4.
    Bartlett JG (2002) Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 346:334–339PubMedCrossRefGoogle Scholar
  5. 5.
    Bassetti S, Frei R, Zimmerli W (1998) Fungemia with Saccharomyces cerevisiae after treatment with S. boulardii. Am J Med 105:71–72PubMedCrossRefGoogle Scholar
  6. 6.
    Baumgart D (2007) The probiotic yeast Saccharomyces boulardii inhibits DC-induced activation of naïve T-cells. Gastroenterology 135(4):A–559 (sup 1)Google Scholar
  7. 7.
    Benhamou PH, Berlier P, Danjou G et al (1999) Antibiotic-associated diarrhoea in children: a computer monitored double-blind outpatients trial comparing a protective and a probiotic agent. Med Chir Dig 28:163–168Google Scholar
  8. 8.
    Bernet MF, Brassart D, Neeser JR et al (1994) Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35:483–489PubMedCrossRefGoogle Scholar
  9. 9.
    Bhatia SJ, Kochar N, Abraham P et al (1989) Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro. J Clin Microbiol 27:2328–2330PubMedGoogle Scholar
  10. 10.
    Billoo AG, Memon MA, Khaskheli SA, Murtaza G, Iqbal K, Saeed Shekhani M, Siddiqi AQ (2006) Role of a probiotic (Saccharomyces boulardii) in management and prevention of diarrhoea. World J Gastroenterol 12:4557–4560PubMedGoogle Scholar
  11. 11.
    Bléhaut H, Massot J, Elmer GW et al (1989) Disposition kinetics of Saccharomyces boulardii in man and rat. Biopharm Drug Dispos 10:353–364PubMedCrossRefGoogle Scholar
  12. 12.
    Breves G, Faul K, Schröder B et al (2000) Application of the colon-stimulation technique for studying the effects of Saccharomyes boulardii on basic parameters of porcine cecal microbial metabolism disturbed by Clindamycin. Digestion 61:193–200PubMedCrossRefGoogle Scholar
  13. 13.
    Brunser O (2009) Coincubation of Saccharomyces boulardii with Helicobacter pylori. A Morphological Study (in press)Google Scholar
  14. 14.
    Burkhardt O, Köhnlein T, Pletz M et al (2005) Saccharomyces boulardii induced sepsis: successful therapy with voriconazole after treatment failure with fluconazole. Scand J Infect Dis 37:69–72PubMedCrossRefGoogle Scholar
  15. 15.
    Buts JP, Bernasconi P, Vaerman JP et al (1990) Stimulation of secretory IgA and secretory component of immunoglobulins in small intestine of rats treated with Saccharomyces boulardii. Dig Dis Sci 35:251–256PubMedCrossRefGoogle Scholar
  16. 16.
    Buts JP, Bernasconi P, Van Craynest MP et al (1986) Response of human and rat small intestinal mucosa to oral administration of Saccharomyces boulardii. Pediatr Res 20:192–196PubMedCrossRefGoogle Scholar
  17. 17.
    Buts JP, Corthier G, Delmee M (1993) Saccharomyces boulardii for Clostridium difficile-associated enteropathies in infants. J Pediatr Gastroenterol Nutr 16:419–425PubMedGoogle Scholar
  18. 18.
    Buts JP, De Keyser N, De Raedemaeker L (1994) Saccharomyces boulardii enhances rat intestinal enzyme expression by endoluminal release of polyamines. Pediatr Res 36:522–527PubMedCrossRefGoogle Scholar
  19. 19.
    Buts JP, Duranton B, De Keyser N et al (1998) Premature stimulation of rat sucrase-isomaltase (SI) by exogenous insulin and the analog B-Asp10 is regulated by a receptor-mediated signal triggering SI gene transcription. Pediatr Res 43:585–591PubMedCrossRefGoogle Scholar
  20. 20.
    Buts JP, De Keyser N, Marandi S et al (1999) Saccharomyces boulardii upgrades cellular adaptation after proximal enterectomy in rats. Gut 45:89–96PubMedGoogle Scholar
  21. 21.
    Buts JP, De Keyser N, Stilmant C et al (2002) Saccharomyces boulardii enhances N-terminal peptide hydrolysis in suckling rat small intestine by endoluminal release of a zinc-binding metalloprotease. Pediatr Res 51:528–534PubMedCrossRefGoogle Scholar
  22. 22.
    Buts JP, Dekeyser N, Stilmant C et al (2006) Saccharomyces boulardii produces in rat small intestine a novel protein phosphatase that inhibits Escherichia coli endotoxin by dephosphorylation. Pediatr Res 60:24–29PubMedCrossRefGoogle Scholar
  23. 23.
    Canani RB, Cirillo P, Terrin GA et al (2007) Probiotics for treatment of acute diarrhoea in children: randomised clinical trial of five different preparations. BMJ 335:340–347PubMedCrossRefGoogle Scholar
  24. 24.
    Castagliuolo I, LaMont JT, Nikulasson ST et al (1996) Saccharomyces boulardii protease inhibits Clostridium difficile toxin A effects in the rat ileum. Infect Immun 12:5225–5232Google Scholar
  25. 25.
    Castagliuolo I, Riegler MF, Valenick L et al (1999) Saccharomyces boulardii protease mediates Clostridium difficile toxin A and B effects in human colonic mucosa. Infect Immun 67:302–307PubMedGoogle Scholar
  26. 26.
    Castaneda C, Garcia E, Santa Cruz M, Fernandez M, Monterrey P (1995) Effects of Saccharomyces boulardii in children with chronic diarrhea, especially cases due to giardiasis. Rev Mex Pueric Pediatr 2:12–16Google Scholar
  27. 27.
    Cetina-Sauri G, Busto GS (1994) Therapeutic evaluation of Saccharomyces boulardii in children with acute diarrhea. Ann Ped 6:397–400Google Scholar
  28. 28.
    Cindoruk M, Erkan G, Karakan T et al (2007) Efficacy and safety of Saccharomyces boulardii in the 14-day triple anti-Helicobacter pylori therapy: a prospective randomized placebo-controlled double-blind study. Helicobacter 12:309–316PubMedCrossRefGoogle Scholar
  29. 29.
    Czerucka D, Dahan S, Mograbi B et al (2000) Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli-infected T84 cells. Infect Immun 68:5998–6004PubMedCrossRefGoogle Scholar
  30. 30.
    Czerucka D, Piche T, Rampal P (2007) Review article: yeast as probiotics—Saccharomyces boulardii. Aliment Pharmacol Ther 26:767–778PubMedGoogle Scholar
  31. 31.
    Czerucka D, Rampal P (2002) Experimental effects of Saccharomyces boulardii on diarrheal pathogens. Microbes Infect 4:733–739PubMedCrossRefGoogle Scholar
  32. 32.
    Czerucka D, Roux I, Rampal P (1994) Saccharomyces boulardii inhibits secretagogue-mediated adenosine 3′, 5′-cyclic monophosphate induction in intestinal cells. Gastroenterology 106:65–72PubMedGoogle Scholar
  33. 33.
    Dahan S, Dalmasso G, Imbert V et al (2003) Saccharomyces boulardii interfers with enterohemorragic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun 71:766–773PubMedCrossRefGoogle Scholar
  34. 34.
    Dalmasso G, Cottrez F, Imbert V et al (2006) Saccharomyces boulardii inhibits inflammatory bowel disease by trapping T cells in mesenteric lymph nodes. Gastroenterology 131:1812–1825PubMedCrossRefGoogle Scholar
  35. 35.
    Dalmasso G, Loubat A, Dahan S et al (2006) Saccharomyces boulardii prevents TNF-alpha-induced apoptosis in EHEC-infected T84 cells. Res Microbiol 157:456–465PubMedCrossRefGoogle Scholar
  36. 36.
    de Llanos R, Querol A, Pemán J et al (2006) Food and probiotic strains from the Saccharomyces cerevisiae species as a possible origin of human systemic infections. Int J Food Microbiol 110:286–289PubMedCrossRefGoogle Scholar
  37. 37.
    Desreumeaux P, Rousseaux C (2006) Influence of the intestinal microflora on host immunity in inflammatory bowel disease. In G. Microflora Ed. John Libbey EurotextGoogle Scholar
  38. 38.
    Duman DG, Bor S, Ozütemiz O et al (2005) Efficacy and safety of Saccharomyces boulardii in prevention of antibiotic-associated diarrhoea due to Helicobacter pylori eradication. Eur J Gastroenterol Hepatol 17:1357–1361PubMedCrossRefGoogle Scholar
  39. 39.
    Elmer GW, Corthier G (1991) Modulation of Clostridium difficile induced mortality as a function of the dose and the viability of the Saccharomyces boulardii used as a preventative agent in gnotobiotic mice. Can J Microbiol 37:315–317PubMedGoogle Scholar
  40. 40.
    Elmer GW, McFarland LV, Surawicz CM et al (1999) Behaviour of Saccharomyces boulardii in recurrent Clostridium difficile disease patients. Aliment Pharmacol Ther 13:1663–1668PubMedCrossRefGoogle Scholar
  41. 41.
    Elmer GW, Moyer KA, Vega R et al (1995) Evaluation of Saccharomyces boulardii for patients with HIV-related chronic diarrhoea and in healthy volunteers receiving antifungals. Microecol and Ther 25:23–31Google Scholar
  42. 42.
    Elstner CL, Lindsay AN, Book LS et al (1983) Lack of relationship of Clostridium difficile to antibiotic-associated diarrhea in children. Pediatr Inf Dis 2:364–366Google Scholar
  43. 43.
    Erdeve O, Tiras U, Dallar Y (2004) The probiotic effect of Saccharomyces boulardii in a pediatric age group. J Trop Pediatr 50:234–236PubMedCrossRefGoogle Scholar
  44. 44.
    FAO/WHO (2006) Probiotics in Food. Health and nutritional properties and guidelines for evaluation. FAO Food and Nutrition Paper 85 (ftp://ftp.fao.org/docrep/fao/009/a0512e/a0512e00.pdf)
  45. 45.
    Fietto JLR, Araújo RS, Valadão FN et al (2004) Molecular and physiological comparisons between Saccharomyces cerevisiae and Saccharomyces boulardii. Can J Microbiol 50:615–621PubMedCrossRefGoogle Scholar
  46. 46.
    Gaon D, Garcia H, Winter L et al (2003) Effect of Lactobacillus strains and Saccharomyces boulardii on persistent diarrhea in children. Medicina (B Aires) 63:293–298Google Scholar
  47. 47.
    Gedek BR (1999) Adherence of Escherichia coli serogroup O 157 and the Salmonella typhimurium mutant DT 104 to the surface of Saccharomyces boulardii. Mycoses 42:261–264PubMedCrossRefGoogle Scholar
  48. 48.
    Geyik MF, Aldemir M, Hosoglu S et al (2006) The effects of Saccharomyces boulardii on bacterial translocation in rats with obstructive jaundice. Ann R Coll Surg Engl 88:176–180PubMedCrossRefGoogle Scholar
  49. 49.
    Girard P, Pansart Y, Lorette I et al (2003) Dose–response relationship and mechanism of action of Saccharomyces boulardii in castor oil-induced diarrhea in rats. Dig Dis Sci 48:770–774PubMedCrossRefGoogle Scholar
  50. 50.
    Goldman CG, Barrado DA, Balcarce N et al (2006) Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 22:984–988PubMedCrossRefGoogle Scholar
  51. 51.
    Gotteland M, Poliak L, Cruchet S et al (2005) Effect of regular ingestion of Saccharomyces boulardii plus inulin or Lactobacillus acidophilus LB in children colonized by Helicobacter pylori. Acta Paediatr 94:1747–1751PubMedCrossRefGoogle Scholar
  52. 52.
    Graf C, Gavazzi G (2007) Saccharomyces cerevisiae fungemia in an immunocompromised patient not treated with Saccharomyces boulardii preparation. J Infect 54:310–311PubMedCrossRefGoogle Scholar
  53. 53.
    Guarino A, Albano F, Ashkenazi S et al (2008) The ESPGHAN/ESPID Guidelines for the Management of Acute Gastroenteritis in Children in Europe. J Pediatr Gastroenterol Nutr 46:S81–S122PubMedCrossRefGoogle Scholar
  54. 54.
    Hafeez A, Tariq P, Ali S et al (2002) The efficacy of Saccharomyces boulardii in the treatment of acute watery diarrhea in children: a multicentre randomized controlled trial. J Coll Phys Surg Pakist 12:432–434Google Scholar
  55. 55.
    Hennequin C, Kauffman-Lacroix C, Jobert A et al (2000) Possible role of catheters in Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect Diseases 19:16–20CrossRefGoogle Scholar
  56. 56.
    Hennequin C, Thierry A, Richard GF et al (2001) Microsatellite typing as a new tool for identification of Saccharomyces cerevisiae strains. J Clin Microbiol 39:551–559PubMedCrossRefGoogle Scholar
  57. 57.
    Herek O, Kara IG, Kaleli I (2004) Effects of antibiotics and Saccharomyces boulardii on bacterial translocation in burn injury. Surg Today 34:256–260PubMedCrossRefGoogle Scholar
  58. 58.
    Htwe K, Yee KS, Tin M, Vandenplas Y (2008) Effect of Saccharomyces boulardii in the treatment of acute watery diarrhea in Myanmar children: a randomized controlled study. Am J Trop Med Hyg 78:214–216PubMedGoogle Scholar
  59. 59.
    Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216PubMedCrossRefGoogle Scholar
  60. 60.
    Jawhara S, Poulain D (2007) Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med Mycol 45:691–700PubMedCrossRefGoogle Scholar
  61. 61.
    Klein SM, Elmer GW, McFarland LV et al (1993) Recovery and elimination of the biotherapeutic agent, Saccharomyces boulardii, in healthy human volunteers. Pharm Res 10:1615–1619PubMedCrossRefGoogle Scholar
  62. 62.
    Kotowska M, Albrecht P, Szajewska H (2005) Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in children: a randomized double-blind placebo-controlled trial. Aliment Pharmacol Ther 21:583–590PubMedCrossRefGoogle Scholar
  63. 63.
    Kurugol Z, Koturoglu G (2005) Effects of Saccharomyces boulardii in children with acute diarrhoea. Acta Paediatr 94:44–47PubMedCrossRefGoogle Scholar
  64. 64.
    Lionetti E, Miniello VL, Castellaneta SP et al (2006) Lactobacillus reuteri therapy to reduce side-effects during anti-Helicobacter pylori treatment in children: a randomized placebo controlled trial. Aliment Pharmacol Ther 24:1461–1468PubMedCrossRefGoogle Scholar
  65. 65.
    Luyer MD, Buurman WA, Hadfoune M et al (2005) Strain-specific effects of probiotics on gut barrier integrity following hemorrhagic shock. Infect Immun 73:3686–3692PubMedCrossRefGoogle Scholar
  66. 66.
    Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria—a review. Int J Food Microbiol 105:281–295PubMedCrossRefGoogle Scholar
  67. 67.
    McFarland LV, Surawicz CM, Stamm WE (1990) Risk factors for Clostridium difficile carriage and C. difficile-associated diarrhea in a cohort of hospitalized patients. J Infect Dis 162:678–684PubMedGoogle Scholar
  68. 68.
    McFarland LV (1998) Epidemiology, risk factors and treatments for antibiotic-associated diarrhea. Dig Dis 16:292–307PubMedCrossRefGoogle Scholar
  69. 69.
    Mumy KL, Chen X, Kelly CP et al (2008) Saccharomyces boulardii interferes with Shigella pathogenesis by postinvasion signaling events. Am J Physiol Gastrointest Liver Physiol 294:G599–G609PubMedCrossRefGoogle Scholar
  70. 70.
    Muñoz P, Bouza E, Cuenca-Estrella M et al (2005) Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 40:1625–1634PubMedCrossRefGoogle Scholar
  71. 71.
    Piechno S, Seguin P, Gangneux JP (2007) Saccharomyces boulardii fungal sepsis: beware of the yeast. Can J Anaesth 54:245–246PubMedCrossRefGoogle Scholar
  72. 72.
    Pothoulakis C, Kelly CP, Joshi MA et al (1993) Saccharomyces boulardii inhibits Clostridium difficile toxin A binding and enterotoxicity in rat ileum. Gastroenterology 104:1108–1115PubMedGoogle Scholar
  73. 73.
    Riedel BD, Ghishan FK (1996) Acute diarrhea. In: Walker WA, Durie PR, Hamilton JR, Walker-Smith JA, Watkins JB (eds) Pediatric gastrointestinal disease, 2nd edn. Mosby-Year Book Inc., St. Louis, pp 251–262Google Scholar
  74. 74.
    Rigothier MC, Maccario J, Vuong PN et al (1990) Effects of Saccharomyces boulardii yeast on trophozoites of Entamoeba histolytica in vitro and in cecal amebiasis in young rats. Ann Parasitol Hum Comp 65:51–60PubMedGoogle Scholar
  75. 75.
    Rijnders BJA, Van Wijngaerden E, Verwaest C et al (2000) Saccharomyces fungemia complicating S. boulardii treatment in a non-immunocompromised host. Intensive Care Med 26:825PubMedCrossRefGoogle Scholar
  76. 76.
    Rodrigues ACP, Nardi RM, Bambirra EA et al (1996) Effect of Saccharomyces boulardii against experimental oral infection with Salmonella typhimurium and Shigella flexneri conventional and gnotobiotic mice. J Appl Bacteriol 91:251–256Google Scholar
  77. 77.
    Schneider SM, Girard-Pipau F, Filippi J et al (2005) Effects of Saccharomyces boulardii on fecal short-chain fatty acids and microflora in patients on long-term total enteral nutrition. World J Gastroenterol 11:6165–6169PubMedGoogle Scholar
  78. 78.
    Sougioultzis S, Simeonidis S, Bhaskar KR et al (2006) Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-kappaB-mediated IL-8 gene expression. Biochem Biophys Res Commun 343:69–76PubMedCrossRefGoogle Scholar
  79. 79.
    Sykora J, Valeckova K, Amlerova J et al (2005) Effects of a specially designed fermented milk product containing probiotic Lactobacillus casei DN-114 001 and the eradication of H. pylori in children: a prospective randomized double-blind study. J Clin Gastroenterol 39:692–698PubMedCrossRefGoogle Scholar
  80. 80.
    Szajewska H, Setty M, Mrukowicz J et al (2006) Probiotics in gastrointestinal diseases in children: hard and not-so-hard evidence of efficacy. J Pediatr Gastroenterol Nutr 42:454–475PubMedCrossRefGoogle Scholar
  81. 81.
    Szajewska H, Skórka A, Dylag M (2007) Meta-analysis: Saccharomyces boulardii for treating acute diarrhoea in children. Aliment Pharmacol Ther 25:257–264PubMedGoogle Scholar
  82. 82.
    Temmerman R, Pot B, Huys G et al (2003) Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int J Food Microbiol 81:1–10PubMedCrossRefGoogle Scholar
  83. 83.
    Tong JL, Ran ZH, Shen J et al (2007) Meta-analysis: the effect of supplementation with probiotics on eradication rates and side effects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 25:155–168PubMedCrossRefGoogle Scholar
  84. 84.
    Turck D, Bernet JP, Marx J et al (2003) Incidence and risk factors of oral antibiotic-associated diarrhea in an outpatient pediatric population. J Pediatr Gastroenterol Nutr 37:22–26PubMedCrossRefGoogle Scholar
  85. 85.
    Vandenplas Y, Salvatore S, Vieira M et al (2007) Probiotics in infectious diarrhoea in children: are they indicated? Eur J Pediatr 166:1211–1218PubMedCrossRefGoogle Scholar
  86. 86.
    Villarruel G, Rubio DM, Lopez F et al (2007) Saccharomyces boulardii in acute childhood diarrhea: a randomized controlled study. Acta Paediatr 96:538–541PubMedCrossRefGoogle Scholar
  87. 87.
    WHO (2003) The treatment of diarrhoea. A manual for physicians and other senior health workers. WHO/CAH/03.7 10/03Google Scholar
  88. 88.
    WHO (1995) The treatment of diarrhea. A manual for physicians and other senior health workers; WHO/CDR/95.3. Geneva, World Health OrganizationGoogle Scholar
  89. 89.
    Wiström J, Norrby SR, Myhre EB et al (2001) Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study. J Antimicrob Chemother 47:43–50PubMedCrossRefGoogle Scholar
  90. 90.
    Wu X, Vallance BA, Boyer L et al (2008) Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am J Physiol Gastrointest Liver Physiol 294:G295–G306PubMedCrossRefGoogle Scholar
  91. 91.
    Zunic P, Lacotte J, Pegoix M et al (1991) S. boulardii fungemia. Apropos of a case. Therapie 46:498–499PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Yvan Vandenplas
    • 1
  • Oscar Brunser
    • 2
  • Hania Szajewska
    • 3
  1. 1.Universitair Ziekenhuis Kinderen BrusselVrije Universiteit BrusselBrusselsBelgium
  2. 2.Institute of Nutrition and Food Technology (INTA)U. of ChileSantiagoChile
  3. 3.The Medical University of WarsawWarsawPoland

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