Probiotics for human use

Nutrition Bulletin

Volumn 43, Issue 3, 2018, Pages 212-225

  Sanders, M E ^a   Merenstein, D ^b   Merrifield, C A ^c   Hutkins, R ^d  

^a International Scientific Association for Probiotics and Prebiotics   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

clinical benefit; fermented food; International Scientific Association for Probiotics and Prebiotics; probiotic; regulatory

Indexed keywords

EID: 85051428152     PISSN: 14719827     EISSN: 14673010     Source Type: Journal    
DOI: 10.1111/nbu.12334     Document Type: Review

References (92)

1. van den Akker CHP, van Goudoever JB, Szajewska H et al. (2018) Probiotics for Preterm Infants: a strain specific systematic review and network meta-analysis. Journal of Pediatric Gastroenterology and Nutrition 67: 103–22.
2. AlFaleh K, Anabrees J (2014) Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Systematic Review (4): CD005496.
3. Allen SJ, Wareham K, Wang D et al. (2013) Lactobacilli and bifidobacteria in the prevention of antibiotic-associated diarrhoea and Clostridium difficile diarrhoea in older inpatients (PLACIDE): a randomised, double-blind, placebo-controlled, multicentre trial. Lancet 382: 1249–57.
4. Anukam K, Osazuwa E, Ahonkhai I et al. (2006) 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 and Infection 8: 1450–4.
5. Babio N, Becerra-Tomas N, Martinez-Gonzalez MA et al. (2015) Consumption of yogurt, low-fat milk, and other low-fat dairy products is associated with lower risk of metabolic syndrome incidence in an elderly Mediterranean population. Journal of Nutrition 145: 2308–16.
6. Bartle D, Knight C, Cairns P (2016) The Use of Probiotics in Preterm Babies. In NHS. South West Neonatal Framework NHS. South West Neonatal Framework, pp. 1–7. Available at: http://www.swneonatalnetwork.co.uk/media/89842/swnn-guideline-probiotics-in-preterm-babies-final-January-2016-version-02.pdf (accessed 1 April 2018).
7. Beltran-Barrientos LM, Gonzalez-Cordova AF, Hernandez-Mendoza A et al. (2018) Randomized double-blind controlled clinical trial of the blood pressure-lowering effect of fermented milk with Lactococcus lactis: a pilot study. Journal of Dairy Science 101: 2819–25.
8. Berke R, Singh A & Guralnick M (2012) Atopic dermatitis: an overview. American Family Physician 86: 35–42.
9. Bourreille A, Cadiot G, Le Dreau G et al. (2013) Saccharomyces boulardii does not prevent relapse of Crohn's disease. Clinical Gastroenterology and Hepatology 11: 982–7.
10. Braegger C, Chmielewska A, Decsi T et al. (2011) Supplementation of infant formula with probiotics and/or prebiotics: a systematic review and comment by the ESPGHAN committee on nutrition. Journal of Pediatric Gastroenterology and Nutrition 52: 238–50.
11. Chamlagain B, Sugito TA, Deptula P et al. (2018) In situ production of active vitamin B12 in cereal matrices using Propionibacterium freudenreichii. Food Sciences and Nutrition 6: 67–76.
12. Chiron C, Tompkins TA & Burguiere P (2018) Flow cytometry: a versatile technology for specific quantification and viability assessment of micro-organisms in multistrain probiotic products. Journal of Applied Microbiology 124: 572–84.
13. Cordina C, Shaikh I, Shrestha S et al. (2011) Probiotics in the management of gastrointestinal disease: analysis of the attitudes and prescribing practices of gastroenterologists and surgeons. Journal of Digestive Diseases 12: 489–96.
14. Costeloe K, Hardy P, Juszczak E et al. (2016) Bifidobacterium breve BBG-001 in very preterm infants: a randomised controlled phase 3 trial. Lancet 387: 649–60.
15. Cuello-Garcia CA, Brozek JL, Fiocchi A et al. (2015) Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. The Journal of Allergy and Clinical Immunology 136: 952–61.
16. Dal Bello F, Walter J, Hammes WP et al. (2003) Increased complexity of the species composition of lactic acid bacteria in human feces revealed by alternative incubation condition. Microbial Ecology 45: 455–63.
17. David LA, Maurice CF, Carmody RN et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559–63.
18. De Beer D, Joubert E, Gelderblom WCA et al. (2002) Phenolic compounds: a review of their possible role as in vivo antioxidants of wine. South African Journal for Enology and Viticulture 23: 48–61.
19. Denning TL, Bhatia AM, Kane AF et al. (2017) Pathogenesis of NEC: role of the innate and adaptive immune response. Seminars in Perinatology 41: 15–28.
20. Eaton S, Rees CM & Hall NJ (2017) Current research on the epidemiology, pathogenesis, and management of necrotizing enterocolitis. Neonatology 111: 423–30.
21. EFSA Panel on Dietetic Products (2010) Scientific Opinion on the substantiation of health claims related to live yoghurt cultures and improved lactose digestion (ID 1143, 2976) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA Journal 8: 1763.
22. Eskesen D, Jespersen L, Michelsen B et al. (2015) Effect of the probiotic strain Bifidobacterium animalis subsp. lactis, BB-12(R), on defecation frequency in healthy subjects with low defecation frequency and abdominal discomfort: a randomised, double-blind, placebo-controlled, parallel-group trial. British Journal of Nutrition 114: 1638–46.
23. FAO & WHO (Food and Agricultural Organization of the United Nations and World Health Organization) (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Available at: http://www.isapp.net/Portals/0/docs/FAO-WHO-2001-Probiotics-Report.pdf (accessed 1 April 2018).
24. FAO & WHO (Food and Agricultural Organization of the United Nations and World Health Organization) (2002) Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. Available at: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf (accessed 1 April 2018).
25. Fiocchi A, Pawankar R, Cuello-Garcia C et al. (2015) World allergy organization-McMaster university guidelines for allergic disease prevention (GLAD-P): probiotics. World Allergy Organization Journal 8: 4.
26. Flach J, van der Waal MB, van den Nieuwboer M et al. (2017) The underexposed role of food matrices in probiotic products: reviewing the relationship between carrier matrices and product parameters. Critical Reviews in Food Science and Nutrition. https://doi.org/10.1080/10408398.2017.1334624.
27. Floch MH, Walker WA, Sanders ME et al. (2015) Recommendations for probiotic use–2015 update: proceedings and consensus opinion. Journal of Clinical Gastroenterology 49(Suppl 1): S69–73.
28. Friedman S & Blumberg RS (2014) Inflammatory bowel disease. In: Harrison's Principles of Internal Medicine, (D Kasper, A Fauci, S Hauser, D Longo, J Jameson & J Loscalzo eds), pp. 2258–75. McGraw-Hill: New York, NY.
29. Frost BL, Modi BP, Jaksic T et al. (2017) New medical and surgical insights into neonatal necrotizing enterocolitis: a review. Journal of the American Medical Association Pediatrics 171: 83–8.
30. Ganzle MG (2014) Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiology 37: 2–10.
31. Gephart SM, McGrath JM, Effken JA et al. (2012) Necrotizing enterocolitis risk: state of the science. Advances in Neonatal Care 12: 77–87.
32. Glanville J, King S, Guarner F et al. (2015) A review of the systematic review process and its applicability for use in evaluating evidence for health claims on probiotic foods in the European Union. Nutrition Journal 14: 16.
33. Goldenberg JZ, Ma SS, Saxton JD et al. (2013) Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Systematic Review (12): CD006095.
34. Goldenberg JZ, Lytvyn L, Steurich J et al. (2015) Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Systematic Review (12): CD004827.
35. Guarner F, Sanders ME, Eliakim R et al. (2017) WGO Practice Guideline – Probiotics and Prebiotics, Vol. 2018. World Gastroenterology Organisation: Milwaukee, WI. Available at: http://www.worldgastroenterology.org/guidelines/global-guidelines/probiotics-and-prebiotics (accessed 1 April 2018).
36. Hao Q, Dong BR, Wu T (2015) Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Systematic Review (2): CD006895.
37. Hempel S, Newberry S, Ruelaz A et al. (2011) Safety of probiotics used to reduce risk and prevent or treat disease. Evidence Report Technology Assessment (Full Rep) 200: 1–645.
38. Hill C, Guarner F, Reid G et al. (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology 11: 506–14.
39. Hungin APS, Mitchell CR, Whorwell P et al. (2018) Systematic review: probiotics in the management of lower gastrointestinal symptoms - an updated evidence-based international consensus. Alimentary Pharmacology & Therapeutics 47: 1054–70.
40. Hutkins RW (2006) Microbiology and Technology of Fermented Foods. Blackwell Publishing: Chicago.
41. Johnson JD, Cocker K & Chang E (2015) Infantile colic: recognition and treatment. American Family Physician 92: 577–82.
42. Jones ML, Martoni CJ & Prakash S (2012) Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. European Journal of Clinical Nutrition 66: 1234–41.
43. Kim HJ, Ju SY & Park YK (2017) Kimchi intake and atopic dermatitis in Korean aged 19–49 years: the Korea National Health and Nutrition Examination Survey 2010–2012. Asia Pacific Journal of Clinical Nutrition 26: 914–22.
44. King S, Glanville J, Sanders ME et al. (2014) Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: a systematic review and meta-analysis. British Journal of Nutrition 112: 41–54.
45. Kolacek S, Hojsak I, Berni Canani R et al. (2017) Commercial probiotic products: a call for improved quality control. a position paper by the ESPGHAN Working Group for Probiotics and Prebiotics. Journal of Pediatric Gastroenterology and Nutrition 65: 117–24.
46. Kristensen NB, Bryrup T, Allin KH et al. (2016) Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Medicine 8: 52.
47. Lau CS & Chamberlain RS (2016) Probiotics are effective at preventing Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. International Journal of General Medicine 9: 27–37.
48. LeBlanc JG, Laino JE, del Valle MJ et al. (2011) B-group vitamin production by lactic acid bacteria–current knowledge and potential applications. Journal of Applied Microbiology 111: 1297–309.
49. Lyon C, Colangelo H & DeSanto K (2018) Antibiotic prophylaxis for COPD exacerbations. American Family Physician 97: 527–8.
50. Marco ML, Heeney D, Binda S et al. (2017) Health benefits of fermented foods: microbiota and beyond. Current Opinion in Biotechnology 44: 94–102.
51. Mardini HE & Grigorian AY (2014) Probiotic mix VSL#3 is effective adjunctive therapy for mild to moderately active ulcerative colitis: a meta-analysis. Inflammatory Bowel Diseases 20: 1562–7.
52. Martinez RC, Franceschini SA, Patta MC et al. (2009) Improved cure of bacterial vaginosis with single dose of tinidazole (2 g), Lactobacillus rhamnosus GR-1, and Lactobacillus reuteri RC-14: a randomized, double-blind, placebo-controlled trial. Canadian Journal of Microbiology 55: 133–8.
53. Mozaffarian D, Hao T, Rimm EB et al. (2011) Changes in diet and lifestyle and long-term weight gain in women and men. New England Journal of Medicine 364: 2392–404.
54. Naidoo K, Gordon M, Fagbemi AO et al. (2011) Probiotics for maintenance of remission in ulcerative colitis. Cochrane Database Systematic Review 12: CD007443.
55. Nocerino R, Paparo L, Terrin G et al. (2017) Cow's milk and rice fermented with Lactobacillus paracasei CBA L74 prevent infectious diseases in children: a randomized controlled trial. Clinical Nutrition 36: 118–25.
56. Nozue M, Shimazu T, Sasazuki S et al. (2017) Fermented soy product intake is inversely associated with the development of high blood pressure: the Japan public health center-based prospective study. Journal of Nutrition 147: 1749–56.
57. Oak SJ & Jha R (2018) The effects of probiotics in lactose intolerance: a systematic review. Critical Reviews in Food Science and Nutrition 9: 1–9.
58. ONS (Office for National Statistics) (2017) Deaths involving Clostridium difficile. Available at: http://www.ons.gov.uk/peoplepopulationandcommunity/birthsdeathsandmarriages/deaths/datasets/deathsinvolvingclostridiumdifficilereferencetables (accessed 1 April 2018).
59. O'Toole PW & Cooney JC (2008) Probiotic bacteria influence the composition and function of the intestinal microbiota. Interdisciplinary Perspectives on Infectious Diseases 2008: 175285.
60. O'Toole PW, Marchesi JR & Hill C (2017) Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nature Microbiology 2: 17057.
61. Panigrahi P, Parida S, Nanda NC et al. (2017) A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature 548: 407–12.
62. Park S & Bae JH (2016) Fermented food intake is associated with a reduced likelihood of atopic dermatitis in an adult population (Korean National Health and Nutrition Examination Survey 2012–2013). Nutrition Research 36: 125–33.
63. PHE (Public Health England) (2018) National Statistics. Clostridium difficile infection: monthly data by NHS acute trust. Available at: http://www.gov.uk/government/statistics/clostridium-difficile-infection-monthly-data-by-nhs-acute-trust (accessed 1 April 2018).
64. Praagman J, Dalmeijer GW, van der Schouw YT et al. (2015) The relationship between fermented food intake and mortality risk in the European Prospective Investigation into Cancer and Nutrition-Netherlands cohort. British Journal of Nutrition 113: 498–506.
65. Riley RD, Lambert PC & Abo-Zaid G (2010) Meta-analysis of individual participant data: rationale, conduct, and reporting. British Medical Journal 340: c221.
66. Ritchie ML & Romanuk TN (2012) A meta-analysis of probiotic efficacy for gastrointestinal diseases. PLoS ONE 7: e34938.
67. Sanders ME (2011) Impact of probiotics on colonizing microbiota of the gut. Journal of Clinical Gastroenterology 45(Suppl): S115–9.
68. Sanders ME, Merenstein DJ, Ouwehand AC et al. (2016) Probiotic use in at-risk populations. Journal of the American Pharmacists Association 2003 56: 680–6.
69. Sanders ME, Akkermans LM, Haller D et al. (2010) Safety assessment of probiotics for human use. Gut Microbes 1: 164–85.
70. Sanders ME, Heimbach JT, Pot B et al. (2011) Health claims substantiation for probiotic and prebiotic products. Gut Microbes 2: 127–33.
71. Sanders ME, Benson A, Lebeer S et al. (2018) Shared mechanisms among probiotic taxa: implications for general probiotic claims. Current Opinion in Biotechnology 49: 207–16.
72. Sarkar A, Lehto SM, Harty S et al. (2016) Psychobiotics and the manipulation of bacteria-gut-brain signals. Trends in Neurosciences 39: 763–81.
73. Savino F, Cresi F, Pautasso S et al. (2004) Intestinal microflora in breastfed colicky and non-colicky infants. Acta Paediatrica 93: 825–9.
74. Savino F, Bailo E, Oggero R et al. (2005) Bacterial counts of intestinal Lactobacillus species in infants with colic. Pediatric Allergy and Immunology 16: 72–5.
75. Schaffler H & Breitruck A (2018) Clostridium difficile – From colonization to infection. Frontiers in Microbiology 9: 646.
76. Setford PC, Jeffery DW, Grbin PR et al. (2017) Factors affecting extraction and evolution of phenolic compounds during red wine maceration and the role of process modelling. Trends in Food Science & Technology 69: 106–17.
77. Skokovic-Sunjic D (2018) Clinical Guide to Probiotic Products Available in USA. Alliance for Education on Probiotics. Available at: www.usprobioticguide.com (accessed 1 April 2018).
78. Sonestedt E, Wirfalt E, Wallstrom P et al. (2011) Dairy products and its association with incidence of cardiovascular disease: the Malmo diet and cancer cohort. European Journal of Epidemiology 26: 609–18.
79. Spergel JM (2010) Epidemiology of atopic dermatitis and atopic march in children. Immunology and Allergy Clinics of North America 30: 269–80.
80. Sung V, Hiscock H, Tang ML et al. (2014) Treating infant colic with the probiotic Lactobacillus reuteri: double blind, placebo controlled randomised trial. British Medical Journal 348: g2107.
81. Sung V, D'Amico F, Cabana MD et al. (2018) Lactobacillus reuteri to treat infant colic: a meta-analysis. Pediatrics 141: e20171811.
82. Szajewska H & Kolodziej M (2015) Systematic review with meta-analysis: Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea. Alimentary Pharmacology & Therapeutics 42: 793–801.
83. Szajewska H, Skorka A, Ruszczynski M et al. (2013) Meta-analysis: Lactobacillus GG for treating acute gastroenteritis in children–updated analysis of randomised controlled trials. Alimentary Pharmacology & Therapeutics 38: 467–76.
84. Szajewska H, Guarino A, Hojsak I et al. (2014) Use of probiotics for management of acute gastroenteritis: a position paper by the ESPGHAN working group for probiotics and prebiotics. Journal of Pediatric Gastroenterology and Nutrition 58: 531–9.
85. Szajewska H, Canani RB, Guarino A et al. (2016) Probiotics for the prevention of antibiotic-associated diarrhea in children. Journal of Pediatric Gastroenterology and Nutrition 62: 495–506.
86. Topping DL & Clifton PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81: 1031–64.
87. Tu MY, Chen HL, Tung YT et al. (2015) Short-term effects of kefir-fermented milk consumption on bone mineral density and bone metabolism in a randomized clinical trial of osteoporotic patients. PLoS ONE 10: e0144231.
88. US Food and Drug Administration (2016) Substantiation for Structure/Function Claims Made in Infant Formula Labels and Labeling: Guidance for Industry. Available at: http://www.fda.gov/downloads/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/UCM514642.pdf (accessed 1 April 2018).
89. Versalovic J (2013) The human microbiome and probiotics: implications for pediatrics. Annals of Nutrition & Metabolism 63(Suppl 2): 42–52.
90. Wang L, Guo MJ, Gao Q et al. (2018) The effects of probiotics on total cholesterol: a meta-analysis of randomized controlled trials. Medicine (Baltimore) 97: e9679.
91. Zhang C, Derrien M, Levenez F et al. (2016a) Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME Journal 10: 2235–45.
92. Zhang GQ, Hu HJ, Liu CY et al. (2016b) Probiotics for prevention of atopy and food hypersensitivity in early childhood: a PRISMA-compliant systematic review and meta-analysis of randomized controlled trials. Medicine (Baltimore) 95: e2562.