Pediatric Gastroenterology, Hepatology & Nutrition

The Korean Society of Pediatric Gastroenterology, Hepatology and Nutrition (대한소아소화기영양학회)
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Probiotics in Children: What Is the Evidence?

  • Received : 2017.07.04
  • Accepted : 2017.07.31
  • Published : 2017.09.30
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Abstract

The number of papers discussing probiotics increases tremendously that limits the possibility for primary care physicians and clinicians to stay updated. Therefore, the aim of this paper will be to summarize available evidence of probiotic use in well-defined clinical indications of importance for pediatricians. Based on currently available evidence certain probiotic strains (Lactobacillus rhamnosus GG [LGG] and Saccharomyces boulardii) have proven effect in the treatment of acute gastroenteritis and prevention of antibiotic associated diarrhea. Furthermore, LGG was proven to be effective in prevention of nosocomial diarrhea and respiratory tract infection in day care centers. In conclusion, not all probiotic strains have same efficacy for all clinical indications, therefore, only strains with proven efficacy and safety should be recommended.

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References

  1. Food and Agricultural Organization of the United Nations, World Health Organization. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Corboda: FAO, WHO, 2001.
  2. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014;11:506-14. https://doi.org/10.1038/nrgastro.2014.66
  3. Guarino A, Ashkenazi S, Gendrel D, Lo Vecchio A, Shamir R, Szajewska H, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition/European Society for Pediatric Infectious Diseases evidence-based guidelines for the management of acute gastroenteritis in children in Europe: update 2014. J Pediatr Gastroenterol Nutr 2014;59:132-52. https://doi.org/10.1097/MPG.0000000000000375
  4. Enserink R, Mughini-Gras L, Duizer E, Kortbeek T, Van Pelt W. Risk factors for gastroenteritis in child day care. Epidemiol Infect 2015;143:2707-20. https://doi.org/10.1017/S0950268814003367
  5. Gordon M, Akobeng A. Racecadotril for acute diarrhoea in children: systematic review and meta-analyses. Arch Dis Child 2016;101:234-40. https://doi.org/10.1136/archdischild-2015-309676
  6. Szajewska H, Guarino A, Hojsak I, Indrio F, Kolacek S, Shamir R, et al. Use of probiotics for management of acute gastroenteritis: a position paper by the ESPGHAN Working Group for Probiotics and Prebiotics. J Pediatr Gastroenterol Nutr 2014;58:531-9. https://doi.org/10.1097/MPG.0000000000000320
  7. Allen SJ, Martinez EG, Gregorio GV, Dans LF. Probiotics for treating acute infectious diarrhoea. Cochrane Database Syst Rev 2010;(11):CD003048.
  8. Szajewska H, Skorka A, Ruszczynski M, Gieruszczak-Bialek D. Meta-analysis: Lactobacillus GG for treating acute gastroenteritis in children--updated analysis of randomised controlled trials. Aliment Pharmacol Ther 2013;38:467-76. https://doi.org/10.1111/apt.12403
  9. Dinleyici EC, Eren M, Ozen M, Yargic ZA, Vandenplas Y. Effectiveness and safety of Saccharomyces boulardii for acute infectious diarrhea. Expert Opin Biol Ther 2012;12:395-410. https://doi.org/10.1517/14712598.2012.664129
  10. Rosander A, Connolly E, Roos S. Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol 2008;74:6032-40. https://doi.org/10.1128/AEM.00991-08
  11. Szajewska H, Urbanska M, Chmielewska A, Weizman Z, Shamir R. Meta-analysis: Lactobacillus reuteri strain DSM 17938 (and the original strain ATCC 55730) for treating acute gastroenteritis in children. Benef Microbes 2014;5:285-93. https://doi.org/10.3920/BM2013.0056
  12. Dinleyici EC, Dalgic N, Guven S, Metin O, Yasa O, Kurugol Z, et al. Lactobacillus reuteri DSM 17938 shortens acute infectious diarrhea in a pediatric outpatient setting. J Pediatr (Rio J) 2015;91:392-6. https://doi.org/10.1016/j.jped.2014.10.009
  13. Szajewska H, Canani RB, Guarino A, Hojsak I, Indrio F, Kolacek S, et al. Probiotics for the prevention of antibiotic-associated diarrhea in children. J Pediatr Gastroenterol Nutr 2016;62:495-506. https://doi.org/10.1097/MPG.0000000000001081
  14. Missaghi B, Valenti AJ, Owens RC Jr. Clostridium difficile infection: a critical overview. Curr Infect Dis Rep 2008;10:165-73. https://doi.org/10.1007/s11908-008-0028-5
  15. Slattery J, MacFabe DF, Frye RE. The significance of the enteric microbiome on the development of childhood disease: a review of prebiotic and probiotic therapies in disorders of childhood. Clin Med Insights Pediatr 2016;10:91-107.
  16. 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. https://doi.org/10.1542/peds.104.5.e64
  17. Issa I, Moucari R. Probiotics for antibiotic-associated diarrhea: do we have a verdict? World J Gastroenterol 2014;20:17788-95. https://doi.org/10.3748/wjg.v20.i47.17788
  18. Monto AS. Epidemiology of viral respiratory infections. Am J Med 2002;112 Suppl 6A:4S-12S.
  19. Dellepiane RM, Pavesi P, Patria MF, Laicini E, Di Landro G, Pietrogrande MC. Atopy in preschool Italian children with recurrent respiratory infections. Pediatr Med Chir 2009;31:161-4.
  20. Silverstein M, Sales AE, Koepsell TD. Health care utilization and expenditures associated with child care attendance: a nationally representative sample. Pediatrics 2003;111:e371-5. https://doi.org/10.1542/peds.111.4.e371
  21. Haskins R. Acute illness in day care: how much does it cost? Bull N Y Acad Med 1989;65:319-43.
  22. Hojsak I, Kolacek S. Probiotics and prebiotics in the prevention of respiratory tract infections. In: Orel R, ed. Intestinal microbiota, probiotics and prebiotics. Ljubljana: Institute for Probiotics and Functional Foods, Ltd., 2014:117-28.
  23. Gutierrez-Castrellon P, Lopez-Velazquez G, Diaz-Garcia L, Jimenez-Gutierrez C, Mancilla-Ramirez J, Estevez-Jimenez J, et al. Diarrhea in preschool children and Lactobacillus reuteri: a randomized controlled trial. Pediatrics 2014;133:e904-9. https://doi.org/10.1542/peds.2013-0652
  24. Hatakka K, Savilahti E, Ponka A, Meurman JH, Poussa T, Nase L, et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ 2001;322:1327. https://doi.org/10.1136/bmj.322.7298.1327
  25. Hojsak I, Mocic Pavic A, Kos T, Dumancic J, Kolacek S. Bifidobacterium animalis subsp. lactis in prevention of common infections in healthy children attending day care centers-randomized, double blind, placebo-controlled study. Clin Nutr 2016;35:587-91. https://doi.org/10.1016/j.clnu.2015.05.004
  26. Hojsak I, Snovak N, Abdovic S, Szajewska H, Misak Z, Kolacek S. Lactobacillus GG in the prevention of gastrointestinal and respiratory tract infections in children who attend day care centers: a randomized, double-blind, placebo-controlled trial. Clin Nutr 2010;29: 312-6. https://doi.org/10.1016/j.clnu.2009.09.008
  27. Kumpu M, Kekkonen RA, Kautiainen H, Jarvenpaa S, Kristo A, Huovinen P, et al. Milk containing probiotic Lactobacillus rhamnosus GG and respiratory illness in children: a randomized, double-blind, placebo-controlled trial. Eur J Clin Nutr 2012;66:1020-3. https://doi.org/10.1038/ejcn.2012.62
  28. Leyer GJ, Li S, Mubasher ME, Reifer C, Ouwehand AC. Probiotic effects on cold and influenza-like symptom incidence and duration in children. Pediatrics 2009;124: e172-9. https://doi.org/10.1542/peds.2008-2666
  29. Lin JS, Chiu YH, Lin NT, Chu CH, Huang KC, Liao KW, et al. Different effects of probiotic species/strains on infections in preschool children: a double-blind, randomized, controlled study. Vaccine 2009;27:1073-9. https://doi.org/10.1016/j.vaccine.2008.11.114
  30. Merenstein D, Gonzalez J, Young AG, Roberts RF, Sanders ME, Petterson S. Study to investigate the potential of probiotics in children attending school. Eur J Clin Nutr 2011;65:447-53. https://doi.org/10.1038/ejcn.2010.290
  31. Merenstein D, Murphy M, Fokar A, Hernandez RK, Park H, Nsouli H, et al. Use of a fermented dairy probiotic drink containing Lactobacillus casei (DN-114 001) to decrease the rate of illness in kids: the DRINK study. A patient-oriented, double-blind, cluster-randomized, placebo-controlled, clinical trial. Eur J Clin Nutr 2010;64:669-77. https://doi.org/10.1038/ejcn.2010.65
  32. Merenstein DJ, Smith KH, Scriven M, Roberts RF, Sanders ME, Petterson S. The study to investigate the potential benefits of probiotics in yogurt, a patient-oriented, double-blind, cluster-randomised, placebo-controlled, clinical trial. Eur J Clin Nutr 2010;64:685-91. https://doi.org/10.1038/ejcn.2010.30
  33. Saavedra JM, Abi-Hanna A, Moore N, Yolken RH. Long-term consumption of infant formulas containing live probiotic bacteria: tolerance and safety. Am J Clin Nutr 2004;79:261-7. https://doi.org/10.1093/ajcn/79.2.261
  34. 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. https://doi.org/10.1542/peds.2004-1815
  35. Wang Y, Li X, Ge T, Xiao Y, Liao Y, Cui Y, et al. Probiotics for prevention and treatment of respiratory tract infections in children: a systematic review and metaanalysis of randomized controlled trials. Medicine (Baltimore) 2016;95:e4509. https://doi.org/10.1097/MD.0000000000004509
  36. World Health Organization. Prevention of hospital-acquired infections. 2nd ed. Geneva: World Health Organization, 2002.
  37. World Health Organization. Report on the burden of endemic health care-associated infection worldwide. Geneva: World Health Organization, 2011.
  38. Hojsak I, Abdovic S, Szajewska H, Milosevic M, Krznaric Z, Kolacek S. Lactobacillus GG in the prevention of nosocomial gastrointestinal and respiratory tract infections. Pediatrics 2010;125:e1171-7. https://doi.org/10.1542/peds.2009-2568
  39. Posfay-Barbe KM, Zerr DM, Pittet D. Infection control in paediatrics. Lancet Infect Dis 2008;8:19-31. https://doi.org/10.1016/S1473-3099(07)70310-9
  40. Ejemot-Nwadiaro RI, Ehiri JE, Arikpo D, Meremikwu MM, Critchley JA. Hand washing promotion for preventing diarrhoea. Cochrane Database Syst Rev 2015;(9):CD004265.
  41. Hojsak I, Szajewska H, Canani RB, Guarino A, Indrio F, Kolacek S, et al. Probiotics for the prevention of nosocomial diarrhea in children. J Pediatr Gastroenterol Nutr 2017. doi: 10.1097/MPG.0000000000001637. [Epub ahead of print]
  42. Wanke M, Szajewska H. Lack of an effect of Lactobacillus reuteri DSM 17938 in preventing nosocomial diarrhea in children: a randomized, double-blind, placebo-controlled trial. J Pediatr 2012;161:40-3.e1. https://doi.org/10.1016/j.jpeds.2011.12.049
  43. Urbanska M, Gieruszczak-Bialek D, Szymanski H, Szajewska H. Effectiveness of lactobacillus reuteri DSM 17938 for the prevention of nosocomial diarrhea in children: a randomized, double-blind, placebo-controlled trial. Pediatr Infect Dis J 2016;35:142-5. https://doi.org/10.1097/INF.0000000000000948
  44. Hojsak I, Tokic Pivac V, Mocic Pavic A, Pasini AM, Kolacek S. Bifidobacterium animalis subsp. lactis fails to prevent common infections in hospitalized children: a randomized, double-blind, placebo-controlled study. Am J Clin Nutr 2015;101:680-4. https://doi.org/10.3945/ajcn.114.102004

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