Pediatric Gastroenterology, Hepatology & Nutrition

  • 제27권1호
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  • Pages.1-14
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  • 2024
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  • 2234-8646(pISSN)
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  • 2234-8840(eISSN)
대한소아소화기영양학회 (The Korean Society of Pediatric Gastroenterology, Hepatology and Nutrition)
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Role of Probiotics in the Treatment and Prevention of Common Gastrointestinal Conditions in Children

  • Iva Hojsak (Department of Pediatrics, Referral Center for Pediatric Gastroenterology and Nutrition, Children's Hospital) ;
  • Sanja Kolacek (Department of Pediatrics, Referral Center for Pediatric Gastroenterology and Nutrition, Children's Hospital)
  • 투고 : 2023.04.11
  • 심사 : 2023.08.30
  • 발행 : 2024.01.15
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초록

Probiotics are live microorganisms that confer health benefits to the host when administered in adequate amounts. Although recommendations for probiotic use should be strain-specific, many systematic reviews, including recommendations from different societies, recommend probiotic use in general, providing no relevant information for healthcare professionals regarding which probiotic to recommend for which clinical indication, at what dose, and for how long. This narrative review aimed to present the available evidence on the use of probiotics in the prevention and treatment of common gastrointestinal diseases in children, considering the strain and dose used. Furthermore, this study summarizes the evidence on the possible side effects and quality of products containing probiotics.

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참고문헌

  1. Food and Agricultural Organization of the United Nations and World Health Organization. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria [Internet]. World Health Organization; 2001 [cited 2023 Apr 11]. Available from: https://web.archive.org/web/20121022161702/http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf
  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. Jankiewicz M, Lukasik J, Kotowska M, Kolodziej M, Szajewska H. Strain-specificity of probiotics in pediatrics: a rapid review of the clinical evidence. J Pediatr Gastroenterol Nutr 2023;76:227-31. https://doi.org/10.1097/MPG.0000000000003675
  4. Zheng J, Wittouck S, Salvetti E, Franz C, Harris HMB, Mattarelli P, et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020;70:2782-858. https://doi.org/10.1099/ijsem.0.004107
  5. Guarino A, Aguilar J, Berkley J, Broekaert I, Vazquez-Frias R, Holtz L, et al. Acute gastroenteritis in children of the world: what veeds to be done? J Pediatr Gastroenterol Nutr 2020;70:694-701. https://doi.org/10.1097/MPG.0000000000002669
  6. Szajewska H, Guarino A, Hojsak I, Indrio F, Kolacek S, Orel R, et al. Use of probiotics for the management of acute gastroenteritis in children: an update. J Pediatr Gastroenterol Nutr 2020;71:261-9. https://doi.org/10.1097/MPG.0000000000002751
  7. Guarino A, Ashkenazi S, Gendrel D, Lo Vecchio A, Shamir R, Szajewska H; European Society for Pediatric Gastroenterology, Hepatology, and NutritionEuropean Society for Pediatric Infectious Diseases. 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
  8. Gwee KA, Lee WW, Ling KL, Ooi CJ, Quak SH, Dan YY, et al. Consensus and contentious statements on the use of probiotics in clinical practice: a south east Asian gastro-neuro motility association working team report. J Gastroenterol Hepatol 2018;33:1707-16. https://doi.org/10.1111/jgh.14268
  9. Marchand V. [Using probiotics in the paediatric population]. Paediatr Child Health 2012;17:575-6. English, French. https://doi.org/10.1093/pch/17.10.575
  10. 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
  11. Schnadower D, Tarr PI, Casper TC, Gorelick MH, Dean JM, O'Connell KJ, et al. Lactobacillus rhamnosus GG versus placebo for acute gastroenteritis in children. N Engl J Med 2018;379:2002-14. https://doi.org/10.1056/NEJMoa1802598
  12. Szymanski H, Szajewska H. Lack of efficacy of Lactobacillus reuteri DSM 17938 for the treatment of acute gastroenteritis: a randomized controlled trial. Pediatr Infect Dis J 2019;38:e237-42. https://doi.org/10.1097/INF.0000000000002355
  13. Su GL, Ko CW, Bercik P, Falck-Ytter Y, Sultan S, Weizman AV, et al. AGA clinical practice guidelines on the role of probiotics in the management of gastrointestinal disorders. Gastroenterology 2020;159:697-705. https://doi.org/10.1053/j.gastro.2020.05.059
  14. Freedman SB, Williamson-Urquhart S, Farion KJ, Gouin S, Willan AR, Poonai N, et al. Multicenter trial of a combination probiotic for children with gastroenteritis. N Engl J Med 2018;379:2015-26. https://doi.org/10.1056/NEJMoa1802597
  15. Szajewska H, Berni Canani R, Domellof M, Guarino A, Hojsak I, Indrio F, et al. Probiotics for the management of pediatric gastrointestinal disorders: position paper of the ESPGHAN special interest group on gut microbiota and modifications. J Pediatr Gastroenterol Nutr 2023;76:232-47. https://doi.org/10.1097/MPG.0000000000003633
  16. Barbut F, Lalande V, Burghoffer B, Thien HV, Grimprel E, Petit JC. Prevalence and genetic characterization of toxin A variant strains of Clostridium difficile among adults and children with diarrhea in France. J Clin Microbiol 2002;40:2079-83. https://doi.org/10.1128/JCM.40.6.2079-2083.2002
  17. McFarland LV, Surawicz CM, Stamm WE. Risk factors for Clostridium difficile carriage and C. difficile-associated diarrhea in a cohort of hospitalized patients. J Infect Dis 1990;162:678-84. https://doi.org/10.1093/infdis/162.3.678
  18. 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
  19. Storr M, Stengel A. [Systematic review: clinical evidence of probiotics in the prevention of antibiotic-associated diarrhoea]. MMW Fortschr Med 2021;163 (Suppl 4):19-26. German. https://doi.org/10.1007/s15006-021-9762-5
  20. Hyams JS, Di Lorenzo C, Saps M, Shulman RJ, Staiano A, van Tilburg M. Functional Disorders: Children and Adolescents. Gastroenterology 2016.
  21. Benninga MA, Faure C, Hyman PE, St James Roberts I, Schechter NL, Nurko S. Childhood functional gastrointestinal disorders: neonate/toddler. Gastroenterology 2016;150:1443-55.E2. https://doi.org/10.1053/j.gastro.2016.02.016
  22. Korterink J, Devanarayana NM, Rajindrajith S, Vlieger A, Benninga MA. Childhood functional abdominal pain: mechanisms and management. Nat Rev Gastroenterol Hepatol 2015;12:159-71. https://doi.org/10.1038/nrgastro.2015.21
  23. Hojsak I. Probiotics in functional gastrointestinal disorders. Adv Exp Med Biol 2019;1125:121-37. https://doi.org/10.1007/5584_2018_321
  24. Sung V, D'Amico F, Cabana MD, Chau K, Koren G, Savino F, et al. Lactobacillus reuteri to treat infant colic: a meta-analysis. Pediatrics 2018;141:e20171811.
  25. Nocerino R, De Filippis F, Cecere G, Marino A, Micillo M, Di Scala C, et al. The therapeutic efficacy of Bifidobacterium animalis subsp. lactis BB-12® in infant colic: A randomised, double blind, placebo-controlled trial. Aliment Pharmacol Ther 2020;51:110-20. https://doi.org/10.1111/apt.15561
  26. Chen K, Zhang G, Xie H, You L, Li H, Zhang Y, et al. Efficacy of Bifidobacterium animalis subsp. lactis, BB-12® on infant colic - a randomised, double-blinded, placebo-controlled study. Benef Microbes 2021;12:531-40. https://doi.org/10.3920/BM2020.0233
  27. Romano C, Ferrau' V, Cavataio F, Iacono G, Spina M, Lionetti E, et al. Lactobacillus reuteri in children with functional abdominal pain (FAP). J Paediatr Child Health 2014;50:E68-71. https://doi.org/10.1111/j.1440-1754.2010.01797.x
  28. Weizman Z, Abu-Abed J, Binsztok M. Lactobacillus reuteri DSM 17938 for the management of functional abdominal pain in childhood: a randomized, double-blind, placebo-controlled trial. J Pediatr 2016;174:160-164.e1. https://doi.org/10.1016/j.jpeds.2016.04.003
  29. Jadresin O, Hojsak I, Misak Z, Kekez AJ, Trbojevic T, Ivkovic L, et al. Lactobacillus reuteri DSM 17938 in the treatment of functional abdominal pain in children: RCT study. J Pediatr Gastroenterol Nutr 2017;64:925-9. https://doi.org/10.1097/MPG.0000000000001478
  30. Maragkoudaki M, Chouliaras G, Orel R, Horvath A, Szajewska H, Papadopoulou A. Lactobacillus reuteri DSM 17938 and a placebo both significantly reduced symptoms in children with functional abdominal pain. Acta Paediatr 2017;106:1857-62. https://doi.org/10.1111/apa.13992
  31. Eftekhari K, Vahedi Z, Aghdam MK, Diaz DN. A randomized double-blind placebo-controlled trial of Lactobacillus reuteri for chronic functional abdominal pain in children. Iran J Pediatr 2015;25:e2616.
  32. Trivic I, Niseteo T, Jadresin O, Hojsak I. Use of probiotics in the treatment of functional abdominal pain in children-systematic review and meta-analysis. Eur J Pediatr 2021;180:339-51. https://doi.org/10.1007/s00431-020-03809-y
  33. Xu HL, Zou LL, Chen MB, Wang H, Shen WM, Zheng QH, et al. Efficacy of probiotic adjuvant therapy for irritable bowel syndrome in children: a systematic review and meta-analysis. PLoS One 2021;16:e0255160.
  34. Koppen IJN, Vriesman MH, Saps M, Rajindrajith S, Shi X, van Etten-Jamaludin FS, et al. Prevalence of functional defecation disorders in children: a systematic review and meta-analysis. J Pediatr 2018;198:121-30.e6. https://doi.org/10.1016/j.jpeds.2018.02.029
  35. Benninga MA, Voskuijl WP, Taminiau JAJM. Childhood constipation: is there new light in the tunnel? J Pediatr Gastroenterol Nutr 2004;39:448-64. https://doi.org/10.1002/j.1536-4801.2004.tb00890.x
  36. de Meij TG, de Groot EF, Eck A, Budding AE, Kneepkens CM, Benninga MA, et al. Characterization of microbiota in children with chronic functional constipation. PLoS One 2016;11:e0164731.
  37. Tabbers MM, DiLorenzo C, Berger MY, Faure C, Langendam MW, Nurko S, et al. Evaluation and treatment of functional constipation in infants and children: evidence-based recommendations from ESPGHAN and NASPGHAN. J Pediatr Gastroenterol Nutr 2014;58:258-74. https://doi.org/10.1097/MPG.0000000000000266
  38. Wegh CAM, Baaleman DF, Tabbers MM, Smidt H, Benninga MA. Nonpharmacologic treatment for children with functional constipation: a systematic review and meta-analysis. J Pediatr 2022;240:136-49.e5. https://doi.org/10.1016/j.jpeds.2021.09.010
  39. Warren JR, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983;1:1273-5.
  40. Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 2018;47:868-76. https://doi.org/10.1111/apt.14561
  41. Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, et al. joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in vhildren and adolescents (update 2016). J Pediatr Gastroenterol Nutr 2017;64:991-1003. https://doi.org/10.1097/MPG.0000000000001594
  42. Kato S, Shimizu T, Toyoda S, Gold BD, Ida S, Ishige T, et al. The updated JSPGHAN guidelines for the management of Helicobacter pylori infection in childhood. Pediatr Int 2020;62:1315-31. https://doi.org/10.1111/ped.14388
  43. Graham DY, Javed SU, Keihanian S, Abudayyeh S, Opekun AR. Dual proton pump inhibitor plus amoxicillin as an empiric anti-H. pylori therapy: studies from the United States. J Gastroenterol 2010;45:816-20. https://doi.org/10.1007/s00535-010-0220-x
  44. Lai HH, Lai MW. Treatment of pediatric Helicobacter pylori infection. Antibiotics (Basel) 2022;11:757.
  45. Pacifico L, Osborn JF, Bonci E, Romaggioli S, Baldini R, Chiesa C. Probiotics for the treatment of Helicobacter pylori infection in children. World J Gastroenterol 2014;20:673-83. https://doi.org/10.3748/wjg.v20.i3.673
  46. Lu M, Yu S, Deng J, Yan Q, Yang C, Xia G, et al. Efficacy of probiotic supplementation therapy for Helicobacter pylori eradication: a meta-analysis of randomized controlled trials. PLoS One 2016;11:e0163743.
  47. Feng JR, Wang F, Qiu X, McFarland LV, Chen PF, Zhou R, et al. Efficacy and safety of probiotic-supplemented triple therapy for eradication of Helicobacter pylori in children: a systematic review and network meta-analysis. Eur J Clin Pharmacol 2017;73:1199-208. https://doi.org/10.1007/s00228-017-2291-6
  48. Zhou BG, Chen LX, Li B, Wan LY, Ai YW. Saccharomyces boulardii as an adjuvant therapy for Helicobacter pylori eradication: a systematic review and meta-analysis with trial sequential analysis. Helicobacter 2019;24:e12651.
  49. Fang HR, Zhang GQ, Cheng JY, Li ZY. Efficacy of Lactobacillus-supplemented triple therapy for Helicobacter pylori infection in children: a meta-analysis of randomized controlled trials. Eur J Pediatr 2019;178:7-16. https://doi.org/10.1007/s00431-018-3282-z
  50. Grumet L, Tromp Y, Stiegelbauer V. The development of high-quality multispecies probiotic formulations: from bench to market. Nutrients 2020;12:2453.
  51. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP), Rychen G, Aquilina G, Azimonti G, Bampidis V, Bastos ML, Bories G, et al. Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA J 2018;16:e05206.
  52. European Food Safety Authority. Updated list of QPS-recommended microorganisms for safety risk assessments carried out by EFSA [Internet]. EFSA BIOHAZ Panel; 2023 Jan 25 [cited 2023 Apr 11]. Available from: https://zenodo.org/records/7554079
  53. Food and Drug Administration. Generally Recognized as Safe (GRAS) [Internet]. Food and Drug Administration [cited 2023 Apr 11]. Available from: https://www.fda.gov/food/food-ingredientspackaging/generally-recognized-safe-gras
  54. Hempel S, Newberry S, Ruelaz A, Wang Z, Miles JN, Suttorp MJ, et al. Safety of probiotics used to reduce risk and prevent or treat disease. Evid Rep Technol Assess (Full Rep) 2011;(200):1-645.
  55. Wallace C, Gordon M, Sinopoulou V, Akobeng AK. Probiotics for management of functional abdominal pain disorders in children. Cochrane Database Syst Rev 2023;2:CD012849.
  56. Bafeta A, Koh M, Riveros C, Ravaud P. Harms reporting in randomized controlled trials of interventions aimed at modifying microbiota: a systematic review. Ann Intern Med 2018;169:240-7. https://doi.org/10.7326/M18-0343
  57. Costa RL, Moreira J, Lorenzo A, Lamas CC. Infectious complications following probiotic ingestion: a potentially underestimated problem? a systematic review of reports and case series. BMC Complement Altern Med 2018;18:329.
  58. D'Agostin M, Squillaci D, Lazzerini M, Barbi E, Wijers L, Da Lozzo P. Invasive infections associated with the use of probiotics in children: a systematic review. Children (Basel) 2021;8:924.
  59. Barton LL, Rider ED, Coen RW. Bacteremic infection with Pediococcus: vancomycin-resistant opportunist. Pediatrics 2001;107:775-6. https://doi.org/10.1542/peds.107.4.775
  60. Brecht M, Garg A, Longstaff K, Cooper C, Andersen C. Lactobacillus sepsis following a laparotomy in a preterm infant: a note of caution. Neonatology 2016;109:186-9. https://doi.org/10.1159/000441965
  61. Vallabhaneni S, Walker TA, Lockhart SR, Ng D, Chiller T, Melchreit R, et al. Notes from the field: Fatal gastrointestinal mucormycosis in a premature infant associated with a contaminated dietary supplement--Connecticut, 2014. MMWR Morb Mortal Wkly Rep 2015;64:155-6.
  62. Grzeskowiak L, Isolauri E, Salminen S, Gueimonde M. Manufacturing process influences properties of probiotic bacteria. Br J Nutr 2011;105:887-94. https://doi.org/10.1017/S0007114510004496
  63. Duboux S, Van Wijchen M, Kleerebezem M. The possible link between manufacturing and probiotic efficacy; a molecular point of view on Bifidobacterium. Front Microbiol 2021;12:812536.
  64. Fenster K, Freeburg B, Hollard C, Wong C, Laursen RR, Ouwehand AC. The production and delivery of probiotics: a review of a practical approach. Microorganisms 2019;7:83.
  65. Jackson SA, Schoeni JL, Vegge C, Pane M, Stahl B, Bradley M, et al. Improving end-user trust in the quality of commercial probiotic products. Front Microbiol 2019;10:739.
  66. Sanders ME, Huis in't Veld J. Bringing a probiotic-containing functional food to the market: microbiological, product, regulatory and labeling issues. Antonie Van Leeuwenhoek 1999;76:293-315. https://doi.org/10.1023/A:1002029204834
  67. European Food Safety Authority. Public consultation on the EFSA statement on the requirements for whole genome sequence analysis of microorganisms intentionally used in the food chain [Internet]. European Food Safety Authority; 2020 Jan 16 [cited 2023 Apr 11]. Available from: https://www.efsa.europa.eu/en/consultations/call/public-consultation-efsa-statement-requirements-whole-genome
  68. https://www.fda.gov/animal-veterinary/animal-food-feeds/generally-organized-safe-gras-notificationprogram, http://www.law.umaryland.edu/ProbioticsWhitePaper
  69. Kolacek S, Hojsak I, Canani RB, Guarino A, Indrio F, Orel R, et al. Commercial probiotic products: a call for improved quality control. A position paper by the ESPGHAN working group for probiotics and prebiotics. J Pediatr Gastroenterol Nutr 2017;65:117-24. https://doi.org/10.1097/MPG.0000000000001603
  70. Wang Y, Liang Q, Lu B, Shen H, Liu S, Shi Y, et al. Whole-genome analysis of probiotic product isolates reveals the presence of genes related to antimicrobial resistance, virulence factors, and toxic metabolites, posing potential health risks. BMC Genomics 2021;22:210.
  71. Vecchione A, Celandroni F, Mazzantini D, Senesi S, Lupetti A, Ghelardi E. Compositional quality and potential gastrointestinal behavior of probiotic products commercialized in Italy. Front Med (Lausanne) 2018;5:59.
  72. Vermeulen MJ, Luijendijk A, van Toledo L, van Kaam AH, Reiss IKM. Quality of probiotic products for preterm infants: Contamination and missing strains. Acta Paediatr 2020;109:276-9. https://doi.org/10.1111/apa.14976
  73. Dioso CM, Vital P, Arellano K, Park H, Todorov SD, Ji Y, et al. Do your kids get what you paid for? Evaluation of commercially available probiotic products intended for children in the republic of the philippines and the republic of Korea. Foods 2020;9:1229.