Current Problems in Pediatric and Adolescent Health Care
Volume 38, Issue 10 , Pages 309-327 , November 2008

The Human Microbiome and Probiotics: Implications for Pediatrics

  • Michael H. Hsieh, MD, PhD

      Affiliations

    • Division of Pediatric Urology, Texas Children's Hospital and Scott Department of Urology, Baylor College of Medicine, Houston, Texas
  • ,
  • James Versalovic, MD, PhD

      Affiliations

    • Department of Pathology, Texas Children's Hospital and Baylor College of Medicine, Houston, Texas

References 

  1. Smit AF. The origin of interspersed repeats in the human genome. Curr Opin Genet Dev. 1996;6:743–748
  2. Bock M, Stoye JP. Endogenous retroviruses and the human germline. Curr Opin Genet Dev. 2000;10:651–655
  3. Tierno PM. The secret life of germs (Pocket Books). New York: Atria; 2001;
  4. Paustian T. The normal flora of humans. In:  Paustian T editors. Microbiology and bacteriology: the world of microbes. Madison, WI: University of Wisconsin-Madison; 2006;
  5. Rolfe RD. Interactions among microorganisms of the indigenous intestinal flora and their influence on the host. Rev Infect Dis. 1984;6(Suppl 1):S73–S79
  6. Nackerdien ZE. Perspectives on microbes as oncogenic infectious agents and implications for breast cancer. Med Hypotheses. 2008;71:302–306
  7. Wucherpfennig KW. Structural basis of molecular mimicry. J Autoimmun. 2001;16:293–302
  8. Barbara G, Stanghellini V, Brandi G, Cremon C, Di Nardo G, De Giorgio R, et al. Interactions between commensal bacteria and gut sensorimotor function in health and disease. Am J Gastroenterol. 2005;100:2560–2568
  9. Quigley EM. Germs, gas and the gut; the evolving role of the enteric flora in IBS. Am J Gastroenterol. 2006;101:334–335
  10. Giaffer MH, Holdsworth CD, Duerden BI. The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol. 1991;35:238–243
  11. Nemet-Nejat KR. Daily life in ancient Mesopotamia. In: Westport, Connecticut: Greenwood Publishing Group; 1998;p. 346
  12. Farnsworth ER. Kefir—a complex probiotic. Food Sci Technol Bull Funct Foods. 2005;2:1–17
  13. Versalovic J, Wilson M. Therapeutic microbiology: probiotics and related strategies. In: 1st Edition. Washington, DC: ASM Press; 2008;p. 403
  14. Guidelines for the Evaluation of Probiotics in Food. In: London Ontario, Canada: Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food; 2002;p. 1–11
  15. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638
  16. Gao Z, Tseng CH, Pei Z, Blaser MJ. Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA. 2007;104:2927–2932
  17. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol. 2005;43:3380–3389
  18. Swidsinski A, Loening-Baucke V, Lochs H, Hale LP. Spatial organization of bacterial flora in normal and inflamed intestine: a fluorescence in situ hybridization study in mice. World J Gastroenterol. 2005;11:1131–1140
  19. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol. 2002;68:3401–3407
  20. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449:804–810
  21. Palmer C, Bik EM, Digiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5:e177
  22. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE. 2008;3:e3056
  23. Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, Serrant P, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells?. Pediatrics. 2007;119:e724–e732
  24. Metchnikoff E. The prolongation of life: optimistic studies. New York and London: G.P. Putnam's Sons; 1908;
  25. Fuller R. Probiotics in man and animals. J Appl Bacteriol. 1989;66:365–378
  26. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S. Probiotics: effects on immunity. Am J Clin Nutr. 2001;73:444S–450S
  27. Saavedra JM. Use of probiotics in pediatrics: rationale, mechanisms of action, and practical aspects. Nutr Clin Pract. 2007;22:351–365
  28. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401–1412
  29. Langhendries JP, Detry J, Van Hees J, Lamboray JM, Darimont J, Mozin MJ, et al. Effect of a fermented infant formula containing viable bifidobacteria on the fecal flora composition and pH of healthy full-term infants. J Pediatr Gastroenterol Nutr. 1995;21:177–181
  30. Valeur N, Engel P, Carbajal N, Connolly E, Ladefoged K. Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl Environ Microbiol. 2004;70:1176–1181
  31. Brown JP. Role of gut bacterial flora in nutrition and health: a review of recent advances in bacteriological techniques, metabolism, and factors affecting flora composition. CRC Crit Rev Food Sci Nutr. 1977;8:229–236
  32. Macfarlane S, Macfarlane GT, Cummings JH. Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther. 2006;24:701–714
  33. Haarman M, Knol J. Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol. 2006;72:2359–2365
  34. de Bortoli N, Leonardi G, Ciancia E, Merlo A, Bellini M, Costa F, et al. Helicobacter pylori eradication: a randomized prospective study of triple therapy versus triple therapy plus lactoferrin and probiotics. Am J Gastroenterol. 2007;102:951–956
  35. Francavilla R, Lionetti E, Castellaneta SP, Magista AM, Maurogiovanni G, Bucci N, et al. Inhibition of Helicobacter pylori infection in humans by Lactobacillus reuteri ATCC 55730 and effect on eradication therapy: a pilot study. Helicobacter. 2008;13:127–134
  36. Myllyluoma E, Veijola L, Ahlroos T, Tynkkynen S, Kankuri E, Vapaatalo H, et al. Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapy—a placebo-controlled, double-blind randomized pilot study. Aliment Pharmacol Ther. 2005;21:1263–1272
  37. Nista EC, Candelli M, Cremonini F, Cazzato IA, Zocco MA, Franceschi F, et al. Bacillus clausii therapy to reduce side-effects of anti-Helicobacter pylori treatment: randomized, double-blind, placebo controlled trial. Aliment Pharmacol Ther. 2004;20:1181–1188
  38. Tursi A, Brandimarte G, Giorgetti GM, Modeo ME. Effect of Lactobacillus casei supplementation on the effectiveness and tolerability of a new second-line 10-day quadruple therapy after failure of a first attempt to cure Helicobacter pylori infection. Med Sci Monit. 2004;10:CR662–CR666
  39. Sykora J, Valeckova K, Amlerova J, Siala K, Dedek P, Watkins S, et al. 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. 2005;39:692–698
  40. Weizman Z, Asli G, Alsheikh A. Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics. 2005;115:5–9
  41. Shornikova AV, Casas IA, Isolauri E, Mykkanen H, Vesikari T. Lactobacillus reuteri as a therapeutic agent in acute diarrhea in young children. J Pediatr Gastroenterol Nutr. 1997;24:399-204
  42. Villarruel G, Rubio DM, Lopez F, Cintioni J, Gurevech R, Romero G, et al. Saccharomyces boulardii in acute childhood diarrhoea: a randomized, placebo-controlled study. Acta Paediatr. 2007;96:538–541
  43. Shornikova AV, Casas IA, Mykkanen H, Salo E, Vesikari T. Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis. Pediatr Infect Dis J. 1997;16:1103–1107
  44. Majamaa H, Isolauri E, Saxelin M, Vesikari T. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr. 1995;20:333–338
  45. Oberhelman RA, Gilman RH, Sheen P, Taylor DN, Black RE, Cabrera L, et al. A placebo-controlled trial of Lactobacillus GG to prevent diarrhea in undernourished Peruvian children. J Pediatr. 1999;134:15–20
  46. Salazar-Lindo E, Miranda-Langschwager P, Campos-Sanchez M, Chea-Woo E, Sack RB. Lactobacillus casei strain GG in the treatment of infants with acute watery diarrhea: a randomized, double-blind, placebo controlled clinical trial [ISRCTN67363048]. BMC Pediatr. 2004;4:18
  47. Rosenfeldt V, Michaelsen KF, Jakobsen M, Larsen CN, Moller PL, Tvede M, et al. Effect of probiotic Lactobacillus strains on acute diarrhea in a cohort of nonhospitalized children attending day-care centers. Pediatr Infect Dis J. 2002;21:417–419
  48. Arvola T, Laiho K, Torkkeli S, Mykkanen H, Salminen S, Maunula L, et al. Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study. Pediatrics. 1999;104:e64
  49. Vanderhoof JA, Whitney DB, Antonson DL, Hanner TL, Lupo JV, Young RJ. Lactobacillus GG in the prevention of antibiotic-associated diarrhea in children. J Pediatr. 1999;135:564–568
  50. La Rosa M, Bottaro G, Gulino N, Gambuzza F, Di Forti F, Ini G, et al. [Prevention of antibiotic-associated diarrhea with Lactobacillus sporogens and fructo-oligosaccharides in children (A multicentric double-blind vs placebo study]). Minerva Pediatr. 2003;55:447–452
  51. Can M, Besirbellioglu BA, Avci IY, Beker CM, Pahsa A. Prophylactic Saccharomyces boulardii in the prevention of antibiotic-associated diarrhea: a prospective study. Med Sci Monit. 2006;12:PI19–PI22
  52. Duman DG, Bor S, Ozutemiz O, Sahin T, Oguz D, Istan F, et al. Efficacy and safety of Saccharomyces boulardii in prevention of antibiotic-associated diarrhoea due to Helicobacterpylori eradication. Eur J Gastroenterol Hepatol. 2005;17:1357–1361
  53. Erdeve O, Tiras U, Dallar Y. The probiotic effect of Saccharomyces boulardii in a pediatric age group. J Trop Pediatr. 2004;50:234–236
  54. Kotowska M, Albrecht P, Szajewska H. Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in children: a randomized double-blind placebo-controlled trial. Aliment Pharmacol Ther. 2005;21:583–590
  55. McFarland LV, Surawicz CM, Greenberg RN, Elmer GW, Moyer KA, Melcher SA, et al. Prevention of beta-lactam-associated diarrhea by Saccharomyces boulardii compared with placebo. Am J Gastroenterol. 1995;90:439–448
  56. Surawicz CM, Elmer GW, Speelman P, McFarland LV, Chinn J, van Belle G. Prevention of antibiotic-associated diarrhea by Saccharomyces boulardii: a prospective study. Gastroenterology. 1989;96:981–988
  57. McFarland LV, Surawicz CM, Greenberg RN, Fekety R, Elmer GW, Moyer KA, et al. A randomized placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. JAMA. 1994;271:1913–1918
  58. Saps M, Pensabene L, Di Martino L, Staiano A, Wechsler J, Zheng X, et al. Post-infectious functional gastrointestinal disorders in children. J Pediatr. 2008;152:812–816816e1
  59. Bradley HK, Wyatt GM, Bayliss CE, Hunter JO. Instability in the faecal flora of a patient suffering from food-related irritable bowel syndrome. J Med Microbiol. 1987;23:29–32
  60. Malinen E, Rinttila T, Kajander K, Matto J, Kassinen A, Krogius L, et al. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol. 2005;100:373–382
  61. Kajander K, Myllyluoma E, Rajilic-Stojanovic M, Kyronpalo S, Rasmussen M, Jarvenpaa S, et al. Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota. Aliment Pharmacol Ther. 2008;27:48–57
  62. Kajander K, Hatakka K, Poussa T, Farkkila M, Korpela R. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther. 2005;22:387–394
  63. Kajander K, Krogius-Kurikka L, Rinttila T, Karjalainen H, Palva A, Korpela R. Effects of multispecies probiotic supplementation on intestinal microbiota in irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:463–473
  64. Nobaek S, Johansson ML, Molin G, Ahrne S, Jeppsson B. Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am J Gastroenterol. 2000;95:1231–1238
  65. Fanigliulo L, Comparato G, Aragona G, Cavallaro L, Iori V, Maino M, et al. Role of gut microflora and probiotic effects in the irritable bowel syndrome. Acta Biomed. 2006;77:85–89
  66. O'Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology. 2005;128:541–551
  67. Whorwell PJ, Altringer L, Morel J, Bond Y, Charbonneau D, O'Mahony L, et al. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol. 2006;101:1581–1590
  68. Sinn DH, Song JH, Kim HJ, Lee JH, Son HJ, Chang DK, et al. Therapeutic effect of Lactobacillus acidophilus-SDC 2012, 2013 in patients with irritable bowel syndrome. Dig Dis Sci. 2008;53:2714–2718
  69. Guyonnet D, Chassany O, Ducrotte P, Picard C, Mouret M, Mercier CH, et al. Effect of a fermented milk containing Bifidobacterium animalis DN-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial. Aliment Pharmacol Ther. 2007;26:475–486
  70. Colecchia A, Vestito A, La Rocca A, Pasqui F, Nikiforaki A, Festi D. Effect of a symbiotic preparation on the clinical manifestations of irritable bowel syndrome, constipation-variant (Results of an open, uncontrolled multicenter study). Minerva Gastroenterol Dietol. 2006;52:349–358
  71. Adler SN. The probiotic agent Escherichia coli M-17 has a healing effect in patients with IBS with proximal inflammation of the small bowel. Dig Liver Dis. 2006;38:713
  72. Kim HJ, Vazquez Roque MI, Camilleri M, Stephens D, Burton DD, Baxter K, et al. A randomized controlled trial of a probiotic combination VSL#3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil. 2005;17:687–696
  73. Kim HJ, Camilleri M, McKinzie S, Lempke MB, Burton DD, Thomforde GM, et al. A randomized controlled trial of a probiotic (VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome). Aliment Pharmacol Ther. 2003;17:895–904
  74. Bittner AC, Croffut RM, Stranahan MC. Prescript-assist probiotic-prebiotic treatment for irritable bowel syndrome: a methodologically oriented, 2-week, randomized, placebo-controlled, double-blind clinical study. Clin Ther. 2005;27:755–761
  75. Drouault-Holowacz S, Bieuvelet S, Burckel A, Cazaubiel M, Dray X, Marteau P. A double blind randomized controlled trial of a probiotic combination in 100 patients with irritable bowel syndrome. Gastroenterol Clin Biol. 2008;32:147–152
  76. O'Sullivan MA, O'Morain CA. Bacterial supplementation in the irritable bowel syndrome (A randomised double-blind placebo-controlled crossover study). Dig Liver Dis. 2000;32:294–301
  77. Niv E, Naftali T, Hallak R, Vaisman N. The efficacy of Lactobacillus reuteri ATCC 55730 in the treatment of patients with irritable bowel syndrome—a double blind, placebo-controlled, randomized study. Clin Nutr. 2005;24:925–931
  78. Niedzielin K, Kordecki H, Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol. 2001;13:1143–1147
  79. Sen S, Mullan MM, Parker TJ, Woolner JT, Tarry SA, Hunter JO. Effect of Lactobacillus plantarum 299v on colonic fermentation and symptoms of irritable bowel syndrome. Dig Dis Sci. 2002;47:2615–2620
  80. Bausserman M, Michail S. The use of Lactobacillus GG in irritable bowel syndrome in children: a double-blind randomized control trial. J Pediatr. 2005;147:197–201
  81. Gawronska A, Dziechciarz P, Horvath A, Szajewska H. A randomized double-blind placebo-controlled trial of Lactobacillus GG for abdominal pain disorders in children. Aliment Pharmacol Ther. 2007;25:177–184
  82. Rasquin A, Di Lorenzo C, Forbes D, Guiraldes E, Hyams JS, Staiano A, et al. Childhood functional gastrointestinal disorders: child/adolescent. Gastroenterology. 2006;130:1527–1537
  83. Rousseaux C, Thuru X, Gelot A, Barnich N, Neut C, Dubuquoy L, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med. 2007;13:35–37
  84. Savino F, Pelle E, Palumeri E, Oggero R, Miniero R. Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics. 2007;119:e124–e130
  85. Indrio F, Riezzo G, Raimondi F, Bisceglia M, Cavallo L, Francavilla R. The effects of probiotics on feeding tolerance, bowel habits, and gastrointestinal motility in preterm newborns. J Pediatr. 2008;152:801–806
  86. Stratiki Z, Costalos C, Sevastiadou S, Kastanidou O, Skouroliakou M, Giakoumatou A, et al. The effect of a bifidobacter supplemented bovine milk on intestinal permeability of preterm infants. Early Hum Dev. 2007;83:575–579
  87. Bin-Nun A, Bromiker R, Wilschanski M, Kaplan M, Rudensky B, Caplan M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr. 2005;147:192–196
  88. Lin HC, Su BH, Chen AC, Lin TW, Tsai CH, Yeh TF, et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics. 2005;115:1–4
  89. Schmolzer G, Urlesberger B, Haim M, Kutschera J, Pichler G, Ritschl E, et al. Multi-modal approach to prophylaxis of necrotizing enterocolitis: clinical report and review of literature. Pediatr Surg Int. 2006;22:573–580
  90. Hoyos AB. Reduced incidence of necrotizing enterocolitis associated with enteral administration of Lactobacillus acidophilus and Bifidobacterium infantis to neonates in an intensive care unit. Int J Infect Dis. 1999;3:197–202
  91. Dani C, Biadaioli R, Bertini G, Martelli E, Rubaltelli FF. Probiotics feeding in prevention of urinary tract infection, bacterial sepsis and necrotizing enterocolitis in preterm infants (A prospective double-blind study). Biol Neonate. 2002;82:103–108
  92. Karimi O, Pena AS, van Bodegraven AA. Probiotics (VSL#3) in arthralgia in patients with ulcerative colitis and Crohn's disease: a pilot study. Drugs Today (Barc). 2005;41:453–459
  93. Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, et al. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol. 2005;100:1539–1546
  94. Gionchetti P, Rizzello F, Morselli C, Poggioli G, Tambasco R, Calabrese C, et al. High-dose probiotics for the treatment of active pouchitis. Dis Colon Rectum. 2007;50:2075–2082discussion 2082-4
  95. Kuhbacher T, Ott SJ, Helwig U, Mimura T, Rizzello F, Kleessen B, et al. Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis. Gut. 2006;55:833–841
  96. Tursi A, Brandimarte G, Giorgetti GM, Forti G, Modeo ME, Gigliobianco A. Low-dose balsalazide plus a high-potency probiotic preparation is more effective than balsalazide alone or mesalazine in the treatment of acute mild-to-moderate ulcerative colitis. Med Sci Monit. 2004;10:PI126–PI131
  97. Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers KM, Brigidi P, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology. 2003;124:1202–1209
  98. Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D, Bazzocchi G, et al. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology. 2000;119:305–309
  99. Wildt S, Munck LK, Vinter-Jensen L, Hanse BF, Nordgaard-Lassen I, Christensen S, et al. Probiotic treatment of collagenous colitis: a randomized, double-blind, placebo-controlled trial with Lactobacillus acidophilus and Bifidobacterium animalis subsp (Lactis). Inflamm Bowel Dis. 2006;12:395–401
  100. Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13:912–915
  101. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87:534–538
  102. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213–223
  103. Lee K, Paek K, Lee HY, Park JH, Lee Y. Antiobesity effect of trans-10,cis-12-conjugated linoleic acid-producing Lactobacillus plantarum PL62 on diet-induced obese mice. J Appl Microbiol. 2007;103:1140–1146
  104. Bruce AW, Chadwick P, Hassan A, VanCott GF. Recurrent urethritis in women. Can Med Assoc J. 1973;108:973–976
  105. Bruce AW, Reid G. Probiotics and the urologist. Can J Urol. 2003;10:1785–1789
  106. Kelly MC, Mequio MJ, Pybus V. Inhibition of vaginal lactobacilli by a bacteriocin-like inhibitor produced by Enterococcus faecium 62-6: potential significance for bacterial vaginosis. Infect Dis Obstet Gynecol. 2003;11:147–156
  107. Bacheller CD, Bernstein JM. Urinary tract infections. Med Clin North Am. 1997;81:719–730
  108. Gower PR, Roberts AP. Qualitative assessment of midstream urine cultures in the detection of bacteriuria. Clin Nephrol. 1975;3:10–13
  109. Seno Y, Kariyama R, Mitsuhata R, Monden K, Kumon H. Clinical implications of biofilm formation by Enterococcus faecalis in the urinary tract. Acta Med Okayama. 2005;59:79–87
  110. 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;163:872–877
  111. Saunders S, Bocking A, Challis J, Reid G. Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. Colloids Surf B Biointerfaces. 2007;55:138–142
  112. Chan RC, Bruce AW, Reid G. Adherence of cervical, vaginal and distal urethral normal microbial flora to human uroepithelial cells and the inhibition of adherence of gram-negative uropathogens by competitive exclusion. J Urol. 1984;131:596–601
  113. Reid G, Cook RL, Bruce AW. Examination of strains of lactobacilli for properties that may influence bacterial interference in the urinary tract. J Urol. 1987;138:330–335
  114. Cadieux P, Burton J, Gardiner G, Braunstein I, Bruce AW, Kang CY, et al. Lactobacillus strains and vaginal ecology. JAMA. 2002;287:1940–1941
  115. Colodner R, Edelstein H, Chazan B, Raz R. Vaginal colonization by orally administered Lactobacillus rhamnosus GG. Isr Med Assoc J. 2003;5:767–769
  116. Ocana VS, Elena Nader-Macias M. Production of antimicrobial substances by lactic acid bacteria II: screening bacteriocin-producing strains with probiotic purposes and characterization of a Lactobacillus bacteriocin. Methods Mol Biol. 2004;268:347–353
  117. Osset J, Bartolome RM, Garcia E, Andreu A. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J Infect Dis. 2001;183:485–491
  118. Strus M, Kucharska A, Kukla G, Brzychczy-Wloch M, Maresz K, Heczko PB. The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida. Infect Dis Obstet Gynecol. 2005;13:69–75
  119. 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;12:239–243
  120. Reid G, Bruce AW, Taylor M. Influence of three-day antimicrobial therapy and lactobacillus vaginal suppositories on recurrence of urinary tract infections. Clin Ther. 1992;14:11–16
  121. Reid G, Bruce AW, Taylor M. Instillation of Lactobacillus and stimulation of indigenous organisms to prevent recurrence of urinary tract infections. Microecol Ther. 1995;23:32–45
  122. Bruce AW, Reid G. Intravaginal instillation of lactobacilli for prevention of recurrent urinary tract infections. Can J Microbiol. 1988;34:339–343
  123. Kontiokari T, Laitinen J, Jarvi L, Pokka T, Sundqvist K, Uhari M. Dietary factors protecting women from urinary tract infection. Am J Clin Nutr. 2003;77:600–604
  124. 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;322:1571
  125. Reid G, Charbonneau D, Erb J, Kochanowski B, Beuerman D, Poehner R, et al. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol. 2003;35:131–134
  126. Gerasimov SV. Probiotic prophylaxis in pediatric recurrent urinary tract infections. Clin Pediatr (Phila). 2004;43:95–98
  127. Lee SJ, Shim YH, Cho SJ, Lee JW. Probiotics prophylaxis in children with persistent primary vesicoureteral reflux. Pediatr Nephrol. 2007;22:1315–1320
  128. Anukam K, Osazuwa E, Ahonkhai I, Ngwu M, Osemene G, Bruce AW, et al. Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial. Microbes Infect. 2006;8:1450–1454
  129. Reid G, Kim SO, Kohler GA. Selecting, testing and understanding probiotic microorganisms. FEMS Immunol Med Microbiol. 2006;46:149–157
  130. Kim SO, Sheikh HI, Ha SD, Martins A, Reid G. G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF production in macrophages. Cell Microbiol. 2006;8:1958–1971
  131. Kirjavainen PV, Laine RM, Carter DE, Hammond J-A, Reid G. Expression of anti-microbial defense factors in vaginal mucosa following exposure to Lactobacillus rhamnosus GR-1. Intl J Probiotics Prebiotics. 2008;3:99–106
  132. Velraeds MM, van de Belt-Gritter B, van der Mei HC, Reid G, Busscher HJ. Interference in initial adhesion of uropathogenic bacteria and yeasts to silicone rubber by a Lactobacillus acidophilus biosurfactant. J Med Microbiol. 1998;47:1081–1085
  133. Laughton J, Devillard E, Heinrichs DE, Reid G, McCormick JK. Cell-cell communication in Gram-positive bacteria: inhibition of Staphylococcus aureus exotoxin expression by Lactobacillus reuteri. Banff, Alberta: American Society for Microbiology Conference on cell-cell communication; 2004;
  134. Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, Versalovic J. Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF-kappaB and MAPK signalling. Cell Microbiol. 2008;10:1442–1452
  135. Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J. Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm Bowel Dis. 2008;14:1068–1083
  136. Rook GA. The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders. Trans R Soc Trop Med Hyg. 2007;101:1072–1074
  137. Prescott SL, Dunstan JA, Hale J, Breckler L, Lehmann H, Weston S, et al. Clinical effects of probiotics are associated with increased interferon-gamma responses in very young children with atopic dermatitis. Clin Exp Allergy. 2005;35:1557–1564
  138. Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy. 2008;35:1557–1564
  139. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol. 2007;119:192–198
  140. Kopp MV, Hennemuth I, Heinzmann A, Urbanek R. Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics. 2008;121:e850–e856
  141. Weston S, Halbert A, Richmond P, Prescott SL. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child. 2005;90:892–897
  142. Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy. 2005;60:494–500
  143. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child. 2006;91:814–819
  144. Arslanoglu S, Moro GE, Schmitt J, Tandoi L, Rizzardi S, Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J Nutr. 2008;138:1091–1095
  145. Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol. 1997;99:179–185
  146. Gruber C, Wendt M, Sulser C, Lau S, Kulig M, Wahn U, et al. Randomized, placebo-controlled trial of Lactobacillus rhamnosus GG as treatment of atopic dermatitis in infancy. Allergy. 2007;62:1270–1276
  147. Brouwer ML, Wolt-Plompen SA, Dubois AE, van der Heide S, Jansen DF, Hoijer MA, et al. No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin Exp Allergy. 2006;36:899–906
  148. Folster-Holst R, Muller F, Schnopp N, Abeck D, Kreiselmaier I, Lenz T, et al. Prospective, randomized controlled trial on Lactobacillus rhamnosus in infants with moderate to severe atopic dermatitis. Br J Dermatol. 2006;155:1256–1261
  149. Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain (Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study). Allergy. 2002;57:243–246
  150. Taylor AL, Dunstan JA, Prescott SL. Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol. 2007;119:184–191
  151. Cabana MD, McKean M, Wong AR, Chao C, Caughey AB. Examining the hygiene hypothesis: the Trial of Infant Probiotic Supplementation. Paediatr Perinat Epidemiol. 2007;21(Suppl 3):23–28
  152. Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol. 2003;111:389–395
  153. Passeron T, Lacour JP, Fontas E, Ortonne JP. Prebiotics and synbiotics: two promising approaches for the treatment of atopic dermatitis in children above 2 years. Allergy. 2006;61:431–437
  154. Kalliomaki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet. 2003;361:1869–1871
  155. 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;35:1155–1160
  156. Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. Lactobacillus sepsis associated with probiotic therapy. Pediatrics. 2005;115:178–181
  157. Coeuret V, Gueguen M, Vernoux JP. Numbers and strains of lactobacilli in some probiotic products. Int J Food Microbiol. 2004;97:147–156
  158. Drisko J, Bischoff B, Giles C, Adelson M, Rao RV, McCallum R. Evaluation of five probiotic products for label claims by DNA extraction and polymerase chain reaction analysis. Dig Dis Sci. 2005;50:1113–1117
  159. Elliot E, Teversham K. An evaluation of nine probiotics available in South Africa, August 2003. S Afr Med J. 2004;94:121–124
  160. Hamilton-Miller JM, Shah S, Winkler JT. Public health issues arising from microbiological and labelling quality of foods and supplements containing probiotic microorganisms. Public Health Nutr. 1999;2:223–229
  161. Huys G, Vancanneyt MD, Haene K, Vankerckhoven V, Goossens H, Swings J. Accuracy of species identity of commercial bacterial cultures intended for probiotic or nutritional use. Res Microbiol. 2006;157:803–810
  162. Szajewska H, Fordymacka A, Bardowski J, Gorecki RK, Mrukowicz JZ, Banaszkiewicz A. Microbiological and genetic analysis of probiotic products licensed for medicinal purposes. Med Sci Monit. 2004;10:BR346–BR350
  163. Temmerman R, Scheirlinck I, Huys G, Swings J. Culture-independent analysis of probiotic products by denaturing gradient gel electrophoresis. Appl Environ Microbiol. 2003;69:220–226
  164. Weese JS. Microbiologic evaluation of commercial probiotics. J Am Vet Med Assoc. 2002;220:794–797
  165. Weese JS. Evaluation of deficiencies in labeling of commercial probiotics. Can Vet J. 2003;44:982–983
  166. Drago L, De Vecchi E, Nicola L, Colombo A, Gismondo MR. Microbiological evaluation of commercial probiotic products available in Italy. J Chemother. 2004;16:463–467
  167. Masco L, Huys G, De Brandt E, Temmerman R, Swings J. Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol. 2005;102:221–230

 Dr. Versalovic has received unrestricted research support from Biogaia AB, Stockholm, Sweden, and has received honoraria from Group Danone, Paris, France.

PII: S1538-5442(08)00093-X

doi: 10.1016/j.cppeds.2008.09.001

Current Problems in Pediatric and Adolescent Health Care
Volume 38, Issue 10 , Pages 309-327 , November 2008