A practical guide for probiotics applied to the case of antibiotic-associated diarrhea in The Netherlands

Valeria Agamennone, Cyrille A M Krul, Ger Rijkers, Remco Kort, Valeria Agamennone, Cyrille A M Krul, Ger Rijkers, Remco Kort

Abstract

Background: Antibiotic-associated diarrhea (AAD) is a side-effect frequently associated with the use of broad spectrum antibiotics. Although a number of clinical studies show that co-administration of specific probiotics reduces the risk for AAD, there is still unclarity among healthcare professionals on the recommendation of probiotic products. This paper aims at a practical guide to inform healthcare professionals, patients and consumers about the exact product characteristics of available probiotics with a proven efficacy to prevent AAD.

Methods: The workflow in this paper includes three consecutive steps: 1) systematic review of relevant clinical studies for effective probiotics by a meta-analysis, 2) compilation of a list of available probiotic products, and 3) recommendation of probiotic products that match effective formulations. Our systematic review on the efficacy of probiotics for the prevention of AAD included only studies with randomized, double blind placebo-controlled trials, a clear definition of antibiotic associated diarrhea, and a probiotic administration regime for at least the duration of the antibiotic therapy.

Results: Using our inclusion criteria, we selected 32 out of 128 identified trials and pooled the results of these studies for each specific dairy product and food supplement. The results indicate a total of seven single or multiple-strain formulations favoring the probiotic treatment group, with the strain Lactobacillus rhamnosus GG being the most effective [relative risk ratio of probiotic versus placebo 0.30 (95% CI 0.16-0.5)]. We selected products for recommendation from a compiled list of all probiotic dairy products and food supplements available in The Netherlands and categorized them into groups of products showing effects against the incidence of AAD in at least one, two or three independent clinical studies. We excluded all products which did not unambiguously declare on the label the specific probiotic strain(s) and the number of colony forming units.

Conclusion: Here we present a practical guide that informs healthcare professionals and patients on the availability of probiotic products with a proven efficacy for the prevention of AAD.

Keywords: Antibiotic-associated diarrhea (AAD); Antibiotics; Meta-analysis; Probiotics.

Conflict of interest statement

Not applicable.

Not applicable.

RK is co-founder of the Yoba for Life foundation (2009), a non-profit organization, accredited by the Dutch Tax Authorities as a Public Benevolent Institution (PBI), which aims to promote local production and consumption of fermented products in Africa. African fermented products made with the Yoba starter culture, are not marketed by the foundation as such, but the Yoba for Life foundation stimulates local production and ownership, allowing income-generating activities for African small-scale entrepreneurs in the food sector. The Yoba for Life foundation distributes and sells ready-to-use sachets with dried bacterial starter cultures through a network of partners and volunteers to facilitate the local production of dairy and cereal-based products by controlled bacterial fermentation. The Yoba starter culture contains Lactobacillus rhamnosus yoba 2012, which is a generic variant of Lactobacillus rhamnosus GG. VA, CK and GR declare no competing interests.

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Prescriptions of antibiotics in The Netherlands including those for high risk of AAD. The data have been extracted from the Genees- en hulpmiddelen Informatie Project (GIP; https://www.gipdatabank.nl/databank) from the Zorginstituut Nederland, that collects trends on use of medication in the Netherlands as reported by health insurance companies. Grey bars indicate the antibiotics that are associated with a higher risk of AAD [11, 14–16]
Fig. 2
Fig. 2
Flow diagram of study selection
Fig. 3
Fig. 3
Forest plots of the subgroup meta-analysis of probiotics for AAD (food supplements vs dairy products). Studies are pooled based on composition. Note that we pool all the studies on Saccharomyces boulardii as we consider this to be one strain of Saccharomyces cerevisiae [93]

References

    1. Keeney KM, Yurist-Doutsch S, Arrieta M-C, Finlay BB. Effects of antibiotics on human microbiota and subsequent disease. Annu. Rev. Microbiol. 2014;68:217–235. doi: 10.1146/annurev-micro-091313-103456.
    1. Francino MP. Antibiotics and the human gut microbiome: Dysbioses and accumulation of resistances. Front. Microbiol. 2016;6:1–11. doi: 10.3389/fmicb.2015.01543.
    1. Sarker P, Mily A, Mamun A, Jalal S, Bergman P, Raqib R, et al. Ciprofloxacin affects host cells by suppressing expression of the endogenous antimicrobial peptides cathelicidins and beta-defensin-3 in colon epithelia. Antibiotics. 2014;3:353–374. doi: 10.3390/antibiotics3030353.
    1. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect. Immun. 2009;77:2741–2753. doi: 10.1128/IAI.00006-09.
    1. Jernberg C, Löfmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1:56–66. doi: 10.1038/ismej.2007.3.
    1. Turck D, Bernet J-P, Marx J, Kempf H, Giard P, Walbaum O, et al. Incidence and risk factors of oral antibiotic-associated diarrhea in an outpatient pediatric population. J. Pediatr. Gastroenterol. Nutr. 2003;37:22–26. doi: 10.1097/00005176-200307000-00004.
    1. Wiström J, Norrby SR, Myhre EB, Eriksson S, Granström G, Lagergren L, et al. Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study. J. Antimicrob. Chemother. 2001;47:43–50. doi: 10.1093/jac/47.1.43.
    1. Kramer MS, Hutchinson TA, Naimark L, Contardi R, Flegel KM, Leduc DG. Antibiotic-associated gastrointestinal symptoms in general pediatric outpatients. Pediatrics. 1985;76:365–370.
    1. Kuyvenhoven MM, van Balen FAM, Verheij TJM. Outpatient antibiotic prescriptions from 1992 to 2001 in The Netherlands. J. Antimicrob. Chemother. 2003;52:675–678. doi: 10.1093/jac/dkg412.
    1. GIP/ZorgInstituut Nederland [Internet]. 2016. Available from: . Accessed Feb 2017.
    1. Joint FAO/WHO expert consultation. Health and nutrition properties of probiotics in food including powder milk with live lactic acid bacteria. 2001.
    1. 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;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Ritchie ML. Romanuk TN. A meta-analysis of probiotic efficacy for gastrointestinal diseases. PLoS One. 2012;7:e34938
    1. Lee YK, Puong KY, Ouwehand AC, Salminen S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J. Med. Microbiol. 2003;52:925–930. doi: 10.1099/jmm.0.05009-0.
    1. Von Ossowski I, Reunanen J, Satokari R, Vesterlund S, Kankainen M, Huhtinen H, et al. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl. Environ. Microbiol. 2010;76:2049–2057. doi: 10.1128/AEM.01958-09.
    1. Collado MC, González A, González R, Hernández M, Ferrús MA, Sanz Y. Antimicrobial peptides are among the antagonistic metabolites produced by Bifidobacterium against Helicobacter pylori. Int. J. Antimicrob. Agents. 2005;25:385–391. doi: 10.1016/j.ijantimicag.2005.01.017.
    1. Chu W, Lu F, Zhu W, Kang C. Isolation and characterization of new potential probiotic bacteria based on quorum-sensing system. J. Appl. Microbiol. 2011;110:202–208. doi: 10.1111/j.1365-2672.2010.04872.x.
    1. Cotter PD, Hill C, Ross PR, Paul D, Cotter CH, Bacteriocins RPR. developing innate immunity for food. Nat. Rev. Microbiol. 2005;3:777–788. doi: 10.1038/nrmicro1273.
    1. Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 2004;28:405–440. doi: 10.1016/j.femsre.2004.01.003.
    1. Ashraf R, Shah NP. Immune system stimulation by probiotic microorganisms. Crit. Rev. Food Sci. Nutr. 2014;54:938–956. doi: 10.1080/10408398.2011.619671.
    1. Hempel S, Newberry S, Ruelaz A, Wang Z, Miles JN V, Suttorp MJ, et al. Safety of probiotics used to reduce risk and prevent or treat disease. Evid Rep Technol Assess. 2011;200:1-645.
    1. Snydman DR. The safety of probiotics. Clin. Infect. Dis. 2008;46:S104–S111. doi: 10.1086/523331.
    1. Stadlbauer V. Immunosuppression and probiotics: Are they effective and safe? Benef. Microbes. 2015;6:823–828. doi: 10.3920/BM2015.0065.
    1. Didari T, Solki S, Mozaffari S, Nikfar S, Abdollahi M. A systematic review of the safety of probiotics. Expert Opin. Drug Saf. 2014;13:227–239. doi: 10.1517/14740338.2014.872627.
    1. Sharma P, Tomar SK, Goswami P, Sangwan V, Singh R. Antibiotic resistance among commercially available probiotics. Food Res. Int. 2014;57:176–195. doi: 10.1016/j.foodres.2014.01.025.
    1. Wong A, Ngu DY, Dan LA, Ooi A, Lim RL. Detection of antibiotic resistance in probiotics of dietary supplements. Nutr J. 2015;14:95.
    1. Avadhani A, Miley H. Probiotics for prevention of antibiotic-associated diarrhea and Clostridium difficile-associated disease in hospitalized adults - A meta-analysis. J. Am. Acad. Nurse Pract. 2011;23:269–274. doi: 10.1111/j.1745-7599.2011.00617.x.
    1. Butler CC, Duncan D, Hood K. Does taking probiotics routinely with antibiotics prevent antibiotic associated diarrhoea? BMJ. 2012;344:e682. doi: 10.1136/bmj.e682.
    1. Cremonini F, Di Caro S, Nista EC, Bartolozzi F, Capelli G, Gasbarrini G, et al. Meta-analysis: the effect of probiotic administration on antibiotic-associated diarrhoea. Aliment. Pharmacol. Ther. 2002;16:1461–1467. doi: 10.1046/j.1365-2036.2002.01318.x.
    1. Dendukuri N, Costa V, McGregor M, Brophy JM. Probiotic therapy for the prevention and treatment of Clostridium difficile-associated diarrhea: a systematic review. Can. Med. Assoc. J. 2005;173:167–170. doi: 10.1503/cmaj.050350.
    1. D’Souza AL, Rajkumar C, Cooke J, Bulpitt CJ. Probiotics in prevention of antibiotic associated diarrhoea: meta-analysis. BMJ. 2002;324:1–6.
    1. Goldenberg J, Lytvyn L, Steurich J, Parkin P, Mahant S, Johnston B. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochcrane Database Syst. Rev. 2015;(12):CD004827.
    1. Goldenberg J, Ma S, Saxton J, Martzen M, Vandvik P, Thorlund K, et al. Probiotics for the prevention of Clostridium difficile- associated diarrhea in adults and children. Cochrane Database Syst. Rev. 2013;(12):CD006095.
    1. Hawrelak JA, Whitten DL, Myers SPI. Lactobacillus rhamnosus GG effective in preventing the onset of antibiotic-associated diarrhoea: a systematic review. Digestion. 2005;72:51–56. doi: 10.1159/000087637.
    1. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JNV, Shanman R, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea. Clin. Corner. 2012;307:1959–1969.
    1. Johnston BC, Supina AL, Vohra S. Probiotics for pediatric antibiotic-associated diarrhea: a meta-analysis of randomized placebo-controlled trials. Can. Med. Assoc. J. 2006;175:377–383. doi: 10.1503/cmaj.051603.
    1. Johnston B, Goldenberg J, Vandvik P, Sun X, Guyatt G. Probiotics for the prevention of pediatric antibiotic-associated diarrhea (Cochrane Review). Cochrane Libr. 2011;(11):CD004827.
    1. Johnston BC, Ma SS, Goldenberg JZ, Thorlund K, Vandvik PO, Loeb M, et al. Probiotics for the prevention of Clostridium difficile–associated diarrhea. Ann Intern Med. 2012;157:878–88.
    1. Kale-Pradhan PB, Jassal HK, Wilhelm SM. Role of Lactobacillus in the prevention of antibiotic-associated diarrhea: a meta-analysis. Pharmacotherapy. 2010;30:119–126. doi: 10.1592/phco.30.2.119.
    1. McFarland LV. Probiotics for the primary and secondary prevention of C. difficile infections: A meta-analysis and systematic review. Antibiotics. 2015;4:160–178. doi: 10.3390/antibiotics4020160.
    1. McFarland LV. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am. J. Gastroenterol. 2006;101:812–822. doi: 10.1111/j.1572-0241.2006.00465.x.
    1. McFarland LV. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 2010;16:2202–2222. doi: 10.3748/wjg.v16.i18.2202.
    1. Pattani R, Palda VA, Hwang SW, Shah PS. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile infection among hospitalized patients: systematic review and meta-analysis. Open Med. 2013;7:e56.
    1. Pillai A, Nelson RL. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database Syst. Rev. 2008;(1):CD004611.
    1. Szajewska H, Meta-analysis MJ. Non-pathogenic yeast Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea. Aliment. Pharmacol. Ther. 2005;22:365–372. doi: 10.1111/j.1365-2036.2005.02624.x.
    1. Szajewska H, Kołodziej M. Systematic review with meta-analysis: Lactobacillus rhamnosus GG in the prevention of antibiotic-associated diarrhoea in children and adults. Aliment. Pharmacol. Ther. 2015;42:1149–1157. doi: 10.1111/apt.13404.
    1. Szajewska H, Kołodziej M. Systematic review with meta-analysis: Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea. Aliment. Pharmacol. Ther. 2015;42:793–801. doi: 10.1111/apt.13344.
    1. Szajewska H, Ruszczyński M, Radzikowski A. Probiotics in the prevention of antibiotic-associated diarrhea in children: a meta-analysis of randomized controlled trials. J. Pediatr. 2006;149:367–372. doi: 10.1016/j.jpeds.2006.04.053.
    1. Tung JM, Dolovich LR, Lee CH. Prevention of Clostridium difficile infection with Saccharomyces boulardii: a systematic review. Can. J. Gastroenterol. 2009;23:817–821. doi: 10.1155/2009/915847.
    1. Urbańska M, Gieruszczak-Białek D, Szajewska H. Systematic review with meta-analysis: Lactobacillus reuteri DSM 17938 for diarrhoeal diseases in children. Aliment. Pharmacol. Ther. 2016;43:1025–1034. doi: 10.1111/apt.13590.
    1. Videlock EJ, Cremonini F. Meta-analysis: probiotics in antibiotic-associated diarrhoea. Aliment. Pharmacol. Ther. 2012;35:1355–1369. doi: 10.1111/j.1365-2036.2012.05104.x.
    1. Zou J, Dong J, Meta-Analysis YX. Lactobacillus containing quadruple therapy versus standard triple first-line therapy for Helicobacter pylori eradication. Helicobacter. 2009;14:449–459. doi: 10.1111/j.1523-5378.2009.00716.x.
    1. 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. doi: 10.1097/MPG.0000000000001081.
    1. Suurmond R, van Rhee H, Hak T. Introduction, comparison, and validation of Meta-Essentials: A free and simple tool for meta-analysis. Res. Synth. Methods. 2017;8:537–553. doi: 10.1002/jrsm.1260.
    1. Arvola T, Laiho K, Torkkeli S, Mykka H. Children With Respiratory Infections : A Randomized Study. 1999;104
    1. Beausoleil M, Fortier N, Guénette S, L’Ecuyer A, Savoie M, Franco M, et al. Effect of a fermented milk combining Lactobacillus acidophilus CL1285 and Lactobacillus casei in the prevention of antibiotic-associated diarrhea: A randomized, double-blind, placebo-controlled trial. Can. J. Gastroenterol. 2007;21:732–736. doi: 10.1155/2007/720205.
    1. Cimperman L, Bayless G, Best K, Diligente A, Mordarski B, Oster M, et al. A randomized, double-blind, placebo-controlled pilot study of Lactobacillus reuteri ATCC 55730 for the prevention of antibiotic-associated diarrhea in hospitalized adults. J. Clin. Gastroenterol. 2011;45:785–789. doi: 10.1097/MCG.0b013e3182166a42.
    1. Correa NB, Peret Filho LA, Penna FJ, Lima FM, Nicoli JR. A randomized formula controlled trial of Bifidobacterium lactis and Streptococcus thermophilus for prevention of antibiotic-associated diarrhea in infants. J. Clin. Gastroenterol. 2005;39:385–389. doi: 10.1097/01.mcg.0000159217.47419.5b.
    1. Fox MJ, Ahuja KDK, Robertson IK, Ball MJ, Eri RD. Can probiotic yogurt prevent diarrhoea in children on antibiotics? A double-blind, randomised, placebo-controlled study. BMJ Open. 2015;5:e006474. doi: 10.1136/bmjopen-2014-006474.
    1. Gao XW, Mubasher M, Fang CY, Reifer C, Miller LE. Dose-response efficacy of a proprietary probiotic formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for antibiotic-associated diarrhea and Clostridium difficile-associated diarrhea prophylaxis in adult patient. Am. J. Gastroenterol. 2010;105:1636–1641. doi: 10.1038/ajg.2010.11.
    1. Georgieva M, Pancheva R, Rasheva N, Usheva N, Ivanova L, Koleva K. Use of the probiotic Lactobacillus reuteri DSM 17938 in the prevention of antibiotic-associated infections in hospitalized Bulgarian children: a randomized, controlled trial. J. IMAB - Annu. Proceeding. 2015;21:895–900. doi: 10.5272/jimab.2015214.895.
    1. Hickson M, D’Souza AL, Muthu N, Rogers TR, Want S, Rajkumar C, et al. Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. BMJ. 2007;335:80. doi: 10.1136/bmj.39231.599815.55.
    1. Koning CJ, Jonkers D, Smidt H, Rombouts F, Pennings HJ, Wouters E, et al. The effect of a multispecies probiotic on the composition of the faecal microbiota and bowel habits in chronic obstructive pulmonary disease patients treated with antibiotics. Br J Nutr. 2009;103:1452-60.
    1. Koning CJM, Jonkers DMAE, Stobberingh EE, Mulder L, Rombouts FM, Stockbrügger RW. The effect of a multispecies probiotic on the intestinal microbiota and bowel movements in healthy volunteers taking the antibiotic amoxycillin. Am. J. Gastroenterol. 2008;103:178–189. doi: 10.1111/j.1572-0241.2007.01547.x.
    1. 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. doi: 10.1111/j.1365-2036.2005.02356.x.
    1. Lewis SJ, Potts L, Barry RE. The lack of therapeutic effect of Saccharomyces boulardii in the prevention of antibiotic-related diarrhoea in elderly patients. J. Infect. 1998;36:171–174. doi: 10.1016/S0163-4453(98)80008-X.
    1. Lönnermark E, Friman V, Lappas G, Sandberg T, Berggren A, Adlerberth I. Intake of Lactobacillus plantarum reduces certain gastrointestinal symptoms during treatment with antibiotics. J. Clin. Gastroenterol. 2010;44:106–112. doi: 10.1097/MCG.0b013e3181b2683f.
    1. McFarland L, Surawicz C. Prevention of lactam associated diarrhoea by Saccharomyces boulardii compared with placebo. Am J Gastroenterol. 1995;90:439–448.
    1. 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. doi: 10.1111/j.1365-2036.2005.02448.x.
    1. Pozzoni P, Riva A, Bellatorre A, Amigoni M, Redaelli E, Ronchetti A, et al. Saccharomyces boulardii for the prevention of antibiotic-associated diarrhea in adult hospitalized patients: a single-center, randomized, double-blind, placebo-controlled trial. Am. J. Gastroenterol. 2012;107:922–931. doi: 10.1038/ajg.2012.56.
    1. Ruszczyński M, Radzikowski A, Szajewska H. Clinical trial: Effectiveness of Lactobacillus rhamnosus (strains E/N, Oxy and Pen) in the prevention of antibiotic-associated diarrhoea in children. Aliment. Pharmacol. Ther. 2008;28:154–161. doi: 10.1111/j.1365-2036.2008.03714.x.
    1. Safdar N, Barigala R, Said A, McKinley L. Feasibility and tolerability of probiotics for prevention of antibiotic-associated diarrhoea in hospitalized US military veterans. J. Clin. Pharm. Ther. 2008;33:663–668. doi: 10.1111/j.1365-2710.2008.00980.x.
    1. Sampalis J, Psaradellis E, Rampakakis E. Efficacy of BIO K+ CL1285 in the reduction of antibiotic-associated diarrhea - A placebo controlled double-blind randomized, multi-center study. Arch. Med. Sci. 2010;6:56–64.
    1. Song HJ, Kim J-Y, Jung S-A, Kim S-E, Park H-S, Jeong Y, et al. Effect of probiotic Lactobacillus (Lacidofil® cap) for the prevention of antibiotic-associated diarrhea: a prospective, randomized, double-blind, multicenter study. J. Korean Med. Sci. 2010;25:1784–1791. doi: 10.3346/jkms.2010.25.12.1784.
    1. Surawicz CM, Elmer GW, Speelman P, McFarland L V, Chinn J, Belle VAN. Prevention of antibiotic-associated diarrrhea by Sacchromyces boulardii: A Prospective study. 1989;96:981-88.
    1. Szajewska H, Albrecht P, Topczewska-cabanek A. Randomized, double-blind, placebo-controlled trial: Effect of Lactobacillus GG supplementation on Helicobacter pylori eradication rates and side effects during treatment in children. J Pediatr Gastroenterol Nutr. 2009;431–436.
    1. Szymański H, Armańska M, Kowalska-Duplaga K, Szajewska H. Bifidobacterium longum PL03, Lactobacillus rhamnosus KL53A, and Lactobacillus plantarum PL02 in the prevention of antibiotic-associated diarrhea in children: A randomized controlled pilot trial. Digestion. 2008;78:13–17. doi: 10.1159/000151300.
    1. Tankanow RM, Ross MB, Ertel IJ, Dickinson DG, McCormick LS, Garfinkel JF. A double-blind, placebo-controlled study of the efficacy of Lactinex in the prophylaxis of amoxicillin-induced diarrhea. Dicp. 1990;24:382–384. doi: 10.1177/106002809002400408.
    1. 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. doi: 10.1016/S0022-3476(99)70053-3.
    1. Wenus C, Goll R, Loken EB, Biong AS, Halvorsen DS, Florholmen J. Prevention of antibiotic-associated diarrhoea by a fermented probiotic milk drink. Eur. J. Clin. Nutr. 2008;62:299–301. doi: 10.1038/sj.ejcn.1602718.
    1. Allen SJ, Wareham K, Wang D, Bradley C, Hutchings H, Harris W, et al. 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. 2013;382:1249–1257. doi: 10.1016/S0140-6736(13)61218-0.
    1. Chatterjee S, Kar P, Das T, Ray S, Ganguly S, Rajendiran C, et al. Randomized placebo-controlled double blind multicentric trial on efficacy and safety of Lactobacillus acidophilus LA-5 and Bifidobacterium BB-12 for prevention of antibiotic-associated diarrhea. J. Assoc. Physicians India. 2013;61:708–712.
    1. Evans M, Salewski RP, Christman MC, Girard S-A, Tompkins TA. Effectiveness of Lactobacillus helveticus and Lactobacillus rhamnosus for the management of antibiotic-associated diarrhoea in healthy adults: a randomised, double-blind, placebo-controlled trial. Br. J. Nutr. 2016;116:94–103. doi: 10.1017/S0007114516001665.
    1. Ouwehand AC, DongLian C, Weijian X, Stewart M, Ni J, Stewart T, et al. Probiotics reduce symptoms of antibiotic use in a hospital setting: A randomized dose response study. Vaccine. 2014;32:458–463. doi: 10.1016/j.vaccine.2013.11.053.
    1. Patel J, Curry WJ, Graybill MA, Bernard S, Mcdermott AS, Karpa K. Randomized study of probiotics in primary care. J. Pharm. Heal. Serv. Res. 2014;5:187–190. doi: 10.1111/jphs.12059.
    1. Selinger CP, Bell A, Cairns A, Lockett M, Sebastian S, Haslam N. Probiotic VSL#3 prevents antibiotic-associated diarrhoea in a double-blind, randomized, placebo-controlled clinical trial. J. Hosp. Infect. 2013;84:159–165. doi: 10.1016/j.jhin.2013.02.019.
    1. Douillard FP, Kant R, Ritari J, Paulin L, Palva A, De Vos WM. Comparative genome analysis of Lactobacillus casei strains isolated from Actimel and Yakult products reveals marked similarities and points to a common origin. Microb. Biotechnol. 2013;6:576–587. doi: 10.1111/1751-7915.12062.
    1. Horvath A, Dziechciarz P, Szajewska H. Meta-analysis: Lactobacillus rhamnosus GG for abdominal pain-related functional gastrointestinal disorders in childhood. Aliment. Pharmacol. Ther. 2011;33:1302–1310. doi: 10.1111/j.1365-2036.2011.04665.x.
    1. Sybesma W, Molenaar D, Van IJcken W, Venema K, Korta R. Genome instability in Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 2013;79:2233–2239.
    1. Shen NT, Maw A, Tmanova LL, Pino A, Ancy K, Crawford CV, et al. Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis. Gastroenterology. 2017;152:1889–1900.e9. doi: 10.1053/j.gastro.2017.02.003.
    1. Hayes SR, Vargas AJ. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Explor. J. Sci. Heal. 2016;12:463–466.
    1. Ouwehand AC. A review of dose-responses of probiotics in human studies. Benef. Microbes. 2016:1–10.
    1. Edwards-Ingram L, Gitsham P, Burton N, Warhurst G, Clarke I, Hoyle D, et al. Genotypic and physiological characterization of Saccharomyces boulardii, the probiotic strain of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2007;73:2458–2467. doi: 10.1128/AEM.02201-06.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere