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Meta-Analysis
.2020 Dec 8;12(12):CD003048.
doi: 10.1002/14651858.CD003048.pub4.

Probiotics for treating acute infectious diarrhoea

Affiliations
Meta-Analysis

Probiotics for treating acute infectious diarrhoea

Shelui Collinson et al. Cochrane Database Syst Rev..

Abstract
in English, Persian

Background: Probiotics may be effective in reducing the duration of acute infectious diarrhoea.

Objectives: To assess the effects of probiotics in proven or presumed acute infectious diarrhoea.

Search methods: We searched the trials register of the Cochrane Infectious Diseases Group, MEDLINE, and Embase from inception to 17 December 2019, as well as the Cochrane Controlled Trials Register (Issue 12, 2019), in the Cochrane Library, and reference lists from studies and reviews. We included additional studies identified during external review.

Selection criteria: Randomized controlled trials comparing a specified probiotic agent with a placebo or no probiotic in people with acute diarrhoea that is proven or presumed to be caused by an infectious agent.

Data collection and analysis: Two review authors independently applied inclusion criteria, assessed risk of bias, and extracted data. Primary outcomes were measures of diarrhoea duration (diarrhoea lasting ≥ 48 hours; duration of diarrhoea). Secondary outcomes were number of people hospitalized in community studies, duration of hospitalization in inpatient studies, diarrhoea lasting ≥ 14 days, and adverse events.

Main results: We included 82 studies with a total of 12,127 participants. These studies included 11,526 children (age < 18 years) and 412 adults (three studies recruited 189 adults and children but did not specify numbers in each age group). No cluster-randomized trials were included. Studies varied in the definitions used for "acute diarrhoea" and "end of the diarrhoeal illness" and in the probiotic(s) tested. A total of 53 trials were undertaken in countries where both child and adult mortality was low or very low, and 26 where either child or adult mortality was high. Risk of bias was high or unclear in many studies, and there was marked statistical heterogeneity when findings for the primary outcomes were pooled in meta-analysis. Effect size was similar in the sensitivity analysis and marked heterogeneity persisted. Publication bias was demonstrated from funnel plots for the main outcomes. In our main analysis of the primary outcomes in studies at low risk for all indices of risk of bias, no difference was detected between probiotic and control groups for the risk of diarrhoea lasting ≥ 48 hours (risk ratio (RR) 1.00, 95% confidence interval (CI) 0.91 to 1.09; 2 trials, 1770 participants; moderate-certainty evidence); or for duration of diarrhoea (mean difference (MD) 8.64 hours shorter, 95% CI 29.4 hours shorter to 12.1 hours longer; 6 trials, 3058 participants; very low-certainty evidence). Effect size was similar and marked heterogeneity persisted in pre-specified subgroup analyses of the primary outcomes that included all studies. These included analyses limited to the probiotics Lactobacillus rhamnosus GG and Saccharomyces boulardii. In six trials (433 participants) of Lactobacillus reuteri, there was consistency amongst findings (I² = 0%), but risk of bias was present in all included studies. Heterogeneity also was not explained by types of participants (age, nutritional/socioeconomic status captured by mortality stratum, region of the world where studies were undertaken), diarrhoea in children caused by rotavirus, exposure to antibiotics, and the few studies of children who were also treated with zinc. In addition, there were no clear differences in effect size for the primary outcomes in post hoc analyses according to decade of publication of studies and whether or not trials had been registered. For other outcomes, the duration of hospitalization in inpatient studies on average was shorter in probiotic groups than in control groups but there was marked heterogeneity between studies (I² = 96%; MD -18.03 hours, 95% CI -27.28 to -8.78, random-effects model: 24 trials, 4056 participants). No differences were detected between probiotic and control groups in the number of people with diarrhoea lasting ≥ 14 days (RR 0.49, 95% CI 0.16 to 1.53; 9 studies, 2928 participants) or in risk of hospitalization in community studies (RR 1.26, 95% CI 0.84 to 1.89; 6 studies, 2283 participants). No serious adverse events were attributed to probiotics.

Authors' conclusions: Probiotics probably make little or no difference to the number of people who have diarrhoea lasting 48 hours or longer, and we are uncertain whether probiotics reduce the duration of diarrhoea. This analysis is based on large trials with low risk of bias.

پیشینه: پروبیوتیک‌ها ممکن است در کاهش مدت زمان ابتلا به اسهال عفونی حاد موثر باشند. اهداف: ارزیابی اثرات پروبیوتیک‌ها بر موارد تائید شده یا مشکوک به ابتلا به اسهال عفونی حاد. روش‌های جست‌وجو: پایگاه‌های ثبت کارآزمایی‌های گروه بیماری‌های عفونی در کاکرین، MEDLINE و Embase را از ابتدا تا 17 دسامبر 2019، همچنین پایگاه ثبت کارآزمایی‌های کنترل شده کاکرین (شماره 12، 2019) را در کتابخانه کاکرین، و فهرست منابع مطالعات و مرورها را جست‌وجو کردیم. مطالعات بیشتر که حین مرور خارجی شناسایی شدند، وارد شدند. معیارهای انتخاب: کارآزمایی‌های تصادفی‌سازی و کنترل شده‌ای که به مقایسه یک عامل پروبیوتیک مشخص با دارونما (placebo) یا عدم تجویز پروبیوتیک در افراد مبتلا به اسهال حادی پرداختند که ایجاد آن با یک عامل عفونی، تائید شده یا مشکوک به وجود آن بودند. گردآوری و تجزیه‌وتحلیل داده‌ها: دو نویسنده مرور به‌طور مستقل از هم، معیار واجد شرایط بودن را اعمال، خطر سوگیری (bias) را ارزیابی، و داده‌ها را استخراج کردند. پیامدهای اولیه عبارت بودند از معیارهای مربوط به مدت زمان اسهال (اسهالی که به مدت 48 ساعت یا بیشتر طول بکشد؛ مدت زمان اسهال). پیامدهای ثانویه، تعداد افراد بستری در بیمارستان در مطالعات انجام شده در سطح جامعه، طول مدت بستری در بیمارستان در مطالعات انجام شده روی بیماران بستری، اسهالی که 14 روز یا بیشتر طول بکشد، و عوارض جانبی، بودند. نتایج اصلی: ما 82 مطالعه را، با مجموع 12,127 شرکت‌کننده، وارد کردیم. این مطالعات شامل 11,526 کودک (سن < 18 سال) و 412 بزرگسال بودند (سه مطالعه 189 بزرگسال و کودک را وارد کردند اما تعداد آنها را در هر گروه سنی نشان ندادند). هیچ کارآزمایی تصادفی‌‌سازی شده خوشه‌ای گنجانده نشد. مطالعات در تعاریف استفاده شده برای «اسهال حاد» و «پایان بیماری اسهال» و در پروبیوتیک(های) آزمایش شده، متفاوت بودند. در کل 53 کارآزمایی در کشورهایی انجام شدند که هم مورتالیتی کودکان و هم مورتالیتی بزرگسالان پائین یا بسیار پائین بودند، و 26 مطالعه هم در کشورهایی با مورتالیتی بالای کودکان یا بزرگسالان به سرانجام رسیدند. خطر سوگیری در بسیاری از مطالعات بالا یا نامشخص گزارش شد، و هنگامی که یافته‌های پیامدهای اولیه در متاآنالیز جمع شدند، ناهمگونی آماری قابل توجهی مشخص بود. اندازه تاثیرگذاری درمان در آنالیز حساسیت (sensitivity analysis) مشابه بوده و ناهمگونی مشخصی باقی ماند. سوگیری انتشار از نمودارهای قیفی (funnel plot) برای پیامدهای اصلی نشان داده شد. در آنالیز اصلی ما از پیامدهای اولیه در مطالعات کم‌خطر از نظر همه شاخص‌های خطر سوگیری، هیچ تفاوتی بین گروه‌های پروبیوتیک و کنترل برای خطر ابتلا به اسهالی که به مدت 48 ساعت یا بیشتر طول بکشد (خطر نسبی (RR): 1.00؛ 95% فاصله اطمینان (CI): 0.91 تا 1.09؛ 2 کارآزمایی، 1770 شرکت‌کننده؛ شواهد با قطعیت متوسط) یا برای طول دوره اسهال (تفاوت میانگین (MD): 8.64 ساعت کوتاه‌تر؛ 95% CI؛ 29.4 ساعت کوتاه‌تر تا 12.1 ساعت طولانی‌تر؛ 6 کارآزمایی، 3058 شرکت‌کننده؛ شواهد با قطعیت بسیار پائین)، دیده نشد. اندازه تاثیرگذاری درمان مشابه بوده و ناهمگونی واضحی در آنالیزهای زیرگروه از پیش تعیین شده برای پیامدهای اولیه که شامل تمام مطالعات می‌شد، ادامه داشت. این زیرگروه‌ها شامل آنالیزهای محدود به پروبیوتیک‌های Lactobacillus rhamnosus GG و Saccharomyces boulardii بودند. در شش کارآزمایی (433 شرکت‌کننده) از Lactobacillus reuteri، بین یافته‌ها سازگاری دیده شد (%0 = I²)، اما خطر سوگیری در همه مطالعات وارد شده وجود داشت. ناهمگونی با انواع شرکت‌کنندگان (سن، وضعیت تغذیه‌ای/اجتماعی‌اقتصادی گرفته شده از رتبه مورتالیتی، منطقه‌ای از جهان که مطالعات انجام شدند)، اسهال در کودکان که ناشی از روتاویروس باشد، مصرف آنتی‌بیوتیک‌ها، و چند مطالعه در مورد کودکانی که با روی هم درمان شدند، نیز توجیه نشدند. علاوه بر این، با توجه به دهه زمانی انتشار مطالعات و اینکه کارآزمایی‌ها ثبت شده بودند یا خیر، تفاوت‌های مشخصی در اندازه تاثیرگذاری برای پیامدهای اولیه در آنالیزهای post hoc وجود نداشت. برای سایر پیامدها، طول مدت بستری در بیمارستان در مطالعات انجام شده در شرایط بستری، به‌طور متوسط در گروه‌های پروبیوتیک نسبت به گروه کنترل کمتر بود اما بین مطالعات ناهمگونی واضحی دیده شد (I² = 96%؛ MD؛ 18.03‐ ساعت؛ 95% CI؛ 27.28‐ تا 8.78‐، مدل اثرات تصادفی: 24 کارآزمایی، 4056 شرکت‌کننده). هیچ تفاوتی بین گروه‌های پروبیوتیک و کنترل در تعداد افراد مبتلا به اسهالی که 14 روز یا بیشتر طول کشیده باشد (RR: 0.49؛ 95% CI؛ 0.16 تا 1.53؛ 9 مطالعه، 2928 شرکت‌کننده) یا در معرض خطر بستری شدن در مطالعات انجام شده در سطح جامعه باشند (RR: 1.2؛ 95% CI؛ 0.84 تا 1.89؛ 6 مطالعه، 2283 شرکت‌کننده) دیده نشد. هیچ عارضه جانبی جدی به پروبیوتیک‌ها نسبت داده نشد. نتیجه‌گیری‌های نویسندگان: پروبیوتیک‌ها احتمالا تفاوتی اندک یا عدم تفاوت در تعداد افرادی ایجاد می‌کنند که اسهال آنها 48 ساعت یا بیشتر طول کشیده باشد، و ما مطمئن نیستیم که پروبیوتیک‌ها طول دوره اسهال را کاهش می‌دهند یا خیر. این آنالیز بر اساس یافته‌های کارآزمایی‌های بزرگ با خطر پائین سوگیری انجام شد.

Trial registration: ClinicalTrials.govNCT03539913NCT03684538.

Copyright © 2020 The Authors. Cochrane Database of Systematic Reviews published by John Wiley & Sons, Ltd. on behalf of The Cochrane Collaboration.

PubMed Disclaimer

Conflict of interest statement

Shelui Collinson has no known conflicts of interest.

Andrew Deans has no known conflicts of interest.

April Padua has no known conflicts of interest.

Germana V Gregorio has no known conflicts of interest.

Chao Li has no known conflicts of interest.

Leonila F Dans has no known conflicts of interest.

Stephen J Allen: travel and accommodation expenses to attend the Nutricia Neocate Syneo Meeting (November 2016) at the Nutricia Utrecht Research Centre were paid.

Figures

1
1
Study flow diagram.
2
2
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
3
3
Risk of bias graph: review authors' assessments about each risk of bias item presented as percentages across all included studies.
4
4
Funnel plot of comparison: 1 Primary diarrhoea outcomes, outcome: 1.1 Diarrhoea lasting ≥ 48 hours.
5
5
Funnel plot of comparison: 1 Primary diarrhoea outcomes, outcome: 1.2 Mean duration of diarrhoea.
1.1
1.1. Analysis
Comparison 1: Primary diarrhoea outcomes, Outcome 1: Diarrhoea lasting ≥ 48 hours
1.2
1.2. Analysis
Comparison 1: Primary diarrhoea outcomes, Outcome 2: Mean duration of diarrhoea
2.1
2.1. Analysis
Comparison 2: Secondary diarrhoea outcomes, Outcome 1: Number of people hospitalized in community studies
2.2
2.2. Analysis
Comparison 2: Secondary diarrhoea outcomes, Outcome 2: Duration of hospitalization in inpatient studies
2.3
2.3. Analysis
Comparison 2: Secondary diarrhoea outcomes, Outcome 3: Diarrhoea lasting ≥ 14 days
3.1
3.1. Analysis
Comparison 3: Strain of probiotic organisms, Outcome 1: Diarrhoea lasting ≥ 48 hours
3.2
3.2. Analysis
Comparison 3: Strain of probiotic organisms, Outcome 2: Mean duration of diarrhoea
4.1
4.1. Analysis
Comparison 4: Diarrhoea pathogen: rotavirus, Outcome 1: Mean duration of diarrhoea
5.1
5.1. Analysis
Comparison 5: Age of participants, Outcome 1: Diarrhoea lasting ≥ 48 hours
5.2
5.2. Analysis
Comparison 5: Age of participants, Outcome 2: Mean duration of diarrhoea
6.1
6.1. Analysis
Comparison 6: Severity of diarrhoea (inpatient vs outpatient), Outcome 1: Diarrhoea lasting ≥ 48 hours
6.2
6.2. Analysis
Comparison 6: Severity of diarrhoea (inpatient vs outpatient), Outcome 2: Mean duration of diarrhoea
7.1
7.1. Analysis
Comparison 7: Country mortality stratum, Outcome 1: Diarrhoea lasting ≥ 48 hours
7.2
7.2. Analysis
Comparison 7: Country mortality stratum, Outcome 2: Mean duration of diarrhoea
8.1
8.1. Analysis
Comparison 8: Geographical region, Outcome 1: Diarrhoea lasting ≥ 48 hours
8.2
8.2. Analysis
Comparison 8: Geographical region, Outcome 2: Mean duration of diarrhoea
9.1
9.1. Analysis
Comparison 9: Exposure to antibiotics, Outcome 1: Diarrhoea lasting ≥ 48 hours
9.2
9.2. Analysis
Comparison 9: Exposure to antibiotics, Outcome 2: Duration of diarrhoea
10.1
10.1. Analysis
Comparison 10: Use of zinc, Outcome 1: Duration of diarrhoea
11.1
11.1. Analysis
Comparison 11: Risk of bias, Outcome 1: Diarrhoea lasting ≥ 48 hours
11.2
11.2. Analysis
Comparison 11: Risk of bias, Outcome 2: Mean duration of diarrhoea
12.1
12.1. Analysis
Comparison 12: Publication decade, Outcome 1: Diarrhoea lasting ≥ 48 hours
12.2
12.2. Analysis
Comparison 12: Publication decade, Outcome 2: Mean duration of diarrhoea
13.1
13.1. Analysis
Comparison 13: Prospective trial registration, Outcome 1: Diarrhoea lasting ≥ 48 hours
13.2
13.2. Analysis
Comparison 13: Prospective trial registration, Outcome 2: Mean duration of diarrhoea
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References

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Francavilla 2012 {published data only}
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Freedman 2015 {published data only}
    1. Freedman SB, Sherman PM, Willan A, Johnson D, Gouin S, Schuh S. Emergency department treatment of children with diarrhea who attend day care: a randomized multi dose trial of a Lactobacillus helveticus and Lactobacillus rhamnosus combination probiotic. Clinical Pediatrics 2015;54(12):1158–66. - PubMed
Freedman 2018a {published data only}
    1. 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. New England Journal of Medicine 2018;379(21):2015-26. - PubMed
Guandalini 2000 {published data only}
    1. Guandalini S, Pensabene L, Zikri MA, Dias JA, Casali LB, Hoekstra H, et al. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhoea: a multicenter European trial. Journal of Pediatric Gastroenterology and Nutrition 2000;30(1):54-60. - PubMed
Guarino 1997 {published data only}
    1. Canani RB, Albano F, Spagnuolo MI, Di Benedetto L, Stabile A, Guarino A. Effect of oral administration of Lactobacillus GG on the duration of diarrhea and on rotavirus excretion in ambulatory children (Abstract). Journal of Pediatric Gastroenterology and Nutrition 1997;24(4):469.
    1. Guarino A, Canani RB, Spagnuolo MI, Albano F, Di Benedetto L. Oral bacterial therapy reduces the duration of symptoms and viral excretion in children with mild diarrhoea. Journal of Pediatric Gastroenterology and Nutrition 1997;25(5):516-9. - PubMed
Hamid 2019 {published data only}
    1. Hamid F, Quaium SM, Rahman A, Hussain T, Islam T. Clinical efficacy of Bacillus clausii probiotic in the management of acute diarrhoea in children. Chattogram Maa-O-Shishu Hospital Medical College Journal 2019;18(1):14-7.
Hegar 2015 {published data only}
    1. Hegar B, Waspada IMI, Gunardi H, Vandenplas Y. A double blind randomized trial showing probiotics to be ineffective in acute diarrhea in Indonesian children. Indian Journal of Pediatrics 2015;82(5):410–4. - PubMed
Henker 2007a {published data only}
    1. Henker J, Laass M, Blokhin BM, Bolbot YK, Maydannik VG, Elze M, et al. The probiotic E. coli strain Nissle 1917 (EcN) stops acute diarrhoea in infants and toddlers. European Journal of Paediatrics 2007;166(4):311-8. - PMC - PubMed
Henker 2008 {published data only}
    1. Henker J, Laass MW, Blokhin BM, Maydannik VG, Bolbot YK, Elze M, et al. Probiotic E. coli Nissle 1917 versus placebo for treating diarrhea of greater than 4 days duration in infants and toddlers. Pediatric Infectious Disease Journal 2008;27(6):494-9. - PubMed
Hernandez 1998 {published data only}
    1. Hernandez CL, Pineda EE, Jimenez MIR, Lucena MS. Clinical therapeutic effect of Saccharomyces boulardii on children with acute diarrhea. Revista de Enfermedades Infecciosas en Pediatria 1998;11(43):87-9.
Hochter 1990 {published data only}
    1. Höchter W, Chase D, Hagenhoff G. Saccharomyces boulardii in the treatment of acute adult diarrhoea. [ Saccharomyces boulardii bei acuter Erwachsenendiarrhoea]. Münchener Medizinische Wochenschrift 1990;132(12):188-92.
Hong Chau 2018 {published data only}
    1. Hong Chau TT, Minh Chau NN, Hoang Le NT, Chuang The H, Voong Vinh P, Nguyen To NT, et al. A double blind, randomized, placebo-controlled trial of Lactobacillus acidophilus for the treatment of acute watery diarrhea in Vietnamese children. Pediatric Infectious Disease Journal 2018;37(1):35-42. - PMC - PubMed
Huang 2014 {published data only}
    1. Huang YF, Liu PY, Chen YY, Nong BR, Huang IF, Hsieh KS, Chen KT. Three-combination probiotic therapy in children with Salmonella and rotavirus gastroenteritis. Journal of Clinical Gastroenterology 2014;48(1):37-42. - PubMed
Isolauri 1994 {published data only}
    1. Isolauri E, Kaila M, Mykkanen H, Ling WH, Salminen S. Oral bacteriotherapy for viral gastroenteritis. Digestive Diseases and Sciences 1994;39(12):2595-600. - PubMed
Jasinski 2002 {published data only}
    1. Jasinski C, Tanzi MN, Schelotto F, Varela G, Zanetta E, Acuna AM, et al. Efficacy of Lactobacillus GG in oral rehydration solution [Efectop del Lactobacillus casei administrado en el suero de rehidratacion oral, en el tratamiento de la enfermedad diarreica aguda]. Pediatrika 2002;22(7):231-43.
Javeed 2018 {published data only}
    1. Javeed A, Manzoor S, Wamiq S. Effect of oral Saccharomyces boulardii supplementation on the duration of acute watery diarrhea in children. Pakistan Journal of Medical and Health Sciences 2018;12(1):212-4.
Khan 2017 {published data only}
    1. Khan MA, Khattak MB, Munir A, Naz I. Efficacy of Lactobacillus reuteri in acute watery diarrhea. Medical Forum 2017;28(11):7-11.
Kianifar 2009 {published data only}
    1. Kianifar HR, Farid R, Ahanchian H, Jabbari F, Moghiman T, Sistanian A. Probiotics in the treatment of acute diarrhea in young children. Iranian Journal of Medical Sciences 2009;34(3):204-7.
Kowalska‐Duplaga 1999 {published data only}
    1. Kowalska-Duplaga K, Strus M, Heczko P, Krobicka B, Kurowska-Baran D, Mrukowicz JZ. Lactobif, a marketed probiotic product containing Bifidobacterium ruminantium, was not effective in the treatment of acute rotavirus diarrhoea in infants. Gut 1999;44:17-25.
Kowalska‐Duplaga 2004 {published data only}
    1. Kowalska-Duplaga K, Krzysztof F, Szajewska H, Janiak R. Efficacy of Trilac® in the treatment of acute diarrhoea in infants and young children - a multicentre, randomised, double blind placebo-controlled study. Pediatria Wspolczesna, Gastroenterologia, Hepatologia i Zywienie Dziecka 2004;6(3):295-9.
Kurugol 2005 {published data only}
    1. Kurugol Z, Koturoglu G. Effects of Saccharomyces boulardii in children with acute diarrhoea. Acta Paediatrica 2005;94(1):44-7. - PubMed
Lee 2001 {published data only}
    1. Lee M-C, Lin L-H, Hung K-L, Wu H-Y. Oral bacterial therapy promotes recovery from acute diarrhoea in children. Acta Paediatrica Taiwan 2001;42(5):301-5. - PubMed
Maity 2019 {published data only}
    1. Maity C, Gupta AK. A prospective, interventional, randomized, double-blind, placebo-controlled clinical study to evaluate the efficacy and safety of Bacillus coagulans LBSC in the treatment of acute diarrhea with abdominal discomfort. European Journal of Clinical Pharmacology 2019;75(1):21-31. - PubMed
Mao 2008 {published data only}
    1. Mao M, Yu T, Xiong Y, Wang Z, Liu H, Gotteland M, et al. Effect of a lactose-free milk formula supplemented with bifidobacteria and streptococci on the recovery from acute diarrhoea. Asia Pacific Journal of Clinical Nutrition 2008;17(1):30-4. - PubMed
Narayanappa 2008 {published data only}
    1. Narayanappa D. Randomized double blinded controlled trial to evaluate the efficacy and safety of Bifilac in patients with acute viral diarrhea. Indian Journal of Pediatrics 2008;75(7):709-13. - PubMed
Nixon 2012 {published data only}
    1. Nixon AF, Cunningham SJ, Cohen HW, Crain EF. The effect of Lactobacillus GG (LGG) on acute diarrheal illness in the pediatric emergency department (PED). Pediatric Emergency Care 2012;28(10):1048–51. - PMC - PubMed
Ozkan 2007 {published data only}
    1. Ozkan TB, Sahin E, Erdemir G, Budak F. Effect of Saccharomyces boulardii in children with acute gastroenteritis and its relationship to the immune response. Journal of International Medical Research 2007;35(2):201-12. - PubMed
Pant 1996 {published data only}
    1. Pant AR, Graham SM, Allen SJ, Harikul S, Sabchareon A, Cuevas L, et al. Lactobacillus GG and acute diarrhoea in young children in the tropics. Journal of Tropical Pediatrics 1996;42(3):162-5. - PubMed
Park 2017 {published data only}
    1. Park MS, Kwon B, Ku S, Ji GE. The efficacy of Bifidobacterium longum BORI and Lactobacillus acidophilus AD031 probiotic treatment in infants with rotavirus infection. Nutrients 2017;9:E887. - PMC - PubMed
Phavichitr 2013 {published data only}
    1. Phavichitr N, Puwdee P, Tantibhaedhyangkul R. Cost-benefit analysis of the probiotic treatment of children hospitalized for acute diarrhea in Bangkok, Thailand. Southeast Asian Journal of Tropical Medicine Public Health 2013;44(6):1065-71. - PubMed
Rafeey 2008a {published data only}
    1. Rafeey M, Ostadrahimi A, Boniadi M, Ghorashi Z, Alizadeh MM, Hadafey V. Lactobacillus acidophilus yogurt and supplement in children with acute diarrhea: a clinical trial. Research Journal of Medical Sciences 2008;2(1):13-8.
Raza 1995 {published data only}
    1. Raza S, Graham SM, Allen SJ, Sultana S, Cuevas L, Hart CA. Lactobacillus GG promotes recovery from acute non-bloody diarrhoea in Pakistan. Pediatric Infectious Disease Journal 1995;14(2):107-11. - PubMed
Rerksuppaphol 2010 {published data only}
    1. Rerksuppaphol S, Rerksuppaphol L. Lactobacillus acidophilus and Bifidobacterium bifidum stored at ambient temperature are effective in the treatment of acute diarrhoea. Annals of Tropical Paediatrics 2010;30:299–304. - PMC - PubMed
Riaz 2012 {published data only}
    1. Riaz M, Alam S, Malik A. Efficacy and safety of Saccharomyces boulardii in acute childhood diarrhea: a double blind randomised controlled trial. Indian Journal of Pediatrics 2012;79(4):478–82. - PubMed
Ritchie 2010 {published data only}
    1. Ritchie BK, Brewster DR, Tran CD, Davidson GP, McNeil Y, Butler RN. Efficacy of Lactobacillus GG in Aboriginal children with acute diarrhoeal disease: a randomised clinical trial. Journal of Pediatric Gastroenterology and Nutrition 2010;50(6):619-24. - PubMed
Rosenfeldt 2002a {published data only}
    1. Rosenfeldt V, Michaelsen KF, Jakobsen M, Larsen CN, Moller PL, Pedersen P. Effect of probiotic Lactobacillus strains in young children hospitalized with acute diarrhea. Pediatric Infectious Disease Journal 2002;21(5):411-6. - PubMed
Rosenfeldt 2002b {published data only}
    1. 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. Pediatric Infectious Disease Journal 2002;21(5):417-9. - PubMed
Sarkar 2005 {published data only}
    1. Sarker SA, Sultana S, Fuchs GJ, Alam NH, Azim T, Brűssow H, et al. Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh. Pediatrics 2005;116(2):e221-8. - PubMed
Schnadower 2018 {published data only}
    1. Schnadower D, Tarr PI, Casper TC, Gorelick MH, Dean M, O’Connell KJ, et al. Lactobacillus rhamnosus GG versus placebo for acute gastroenteritis in children. New England Journal of Medicine 2018;379(21):2002-14. - PMC - PubMed
Shornikova 1997a {published data only}
    1. Shornikova AV, Isolauri E, Burkanova L, Lukovnikova S, Vesikari T. A trial in the Karelian Republic of oral rehydration and Lactobacillus GG for treatment of acute diarrhoea. Acta Paediatrica 1997;86(5):460-5. - PubMed
Shornikova 1997b {published data only}
    1. Shornikova AV, Casas IA, Mykkanen H, Salo E, Vesikari T. Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis. Pediatric Infectious Disease Journal 1997;16(12):1103-7. - PubMed
Shornikova 1997c {published data only}
    1. Shornikova AV, Casas IA, Isolauri E, Mykkanen H, Vesikari T. Lactobacillus reuteri as a therapeutic agent in acute diarrhea in young children. Journal of Pediatric Gastroenterology and Nutrition 1997;24(4):399-404. - PubMed
Simadibrata 2013 {published data only}
    1. Simadibrata M, Ndraha S, Tedjasaputra R, Syam AF, Santi AFA, Rani A. Revealing the effect of probiotic combination Lactobacillus rhamnosus and Lactobacillus acidophilus (Lacidofil®) on acute diarrhea in adult patients. Journal of Clinical Medicine and Research 2013;5(2):23-8.
Sirsat 2017 {published data only}
    1. Sirsat GM, Sankpal DM. Role of Saccharomyces boulardii in management of acute diarrhoea of children - A randomized controlled trial. MedPulse International Journal of Pediatrics 2017;4(3):68-72.
Sudha 2019 {published data only}
    1. Sudha MR, Jayanthi N, Pandey DC, Verma AK. Bacillus clausii UBBC-07 reduces severity of diarrhoea in children under 5 years of age: a double blind placebo controlled study. Benef Microbes 2019;10(2):149-54. - PubMed
Szymanski 2006 {published data only}
    1. Szymanski H, Pejcz J, Jawien M, Chmielarczyk A, Strus M, Heczko PB. Treatment of acute infectious diarrhoea in infants and children with a mixture of three Lactobacillus rhamnosus strains -- a randomized, double-blind, placebo-controlled trial. Alimentary Pharmacology and Therapeutics 2006;23(2):247-53. - PubMed
Szymanski 2019 {published data only}
    1. Szymański H, Szajewska H. Lack of efficacy of Lactobacillus reuteri DSM 17938 for the treatment of acute gastroenteritis: a randomized controlled trial. Pediatric Infectious Disease Journal 2019;38(10):e237-42. - PubMed
Teran 2009 {published data only}
    1. Teran CG, Teran-Escalera CN, Villarroel P. Nitazoxanide vs. probiotics for the treatment of acute rotavirus diarrhea in children: a randomized, single-blind, controlled trial in Bolivian children. International Journal of Infectiouos Diseases 2009;13(4):518-23. - PubMed
Urganci 2001 {published data only}
    1. Urganci N, Polat T, Uysalol M, Cetinkaya F. Evaluation of the efficacy of Saccharomyces boulardii in children with acute diarrhoea. Archives of Gastroenterohepatology 2001;20(3-4):81-3.
Vidjeadevan 2018 {published data only}
    1. Vidjeadevan D, Vinoth S, Ramesh S. Role of Saccharomyces boulardii and Bacillus clausii in reducing the duration of diarrhea: a three-armed randomised controlled trial. International Journal of Contemporary Pediatrics 2018;5(5):1811-4.
Villarruel 2007 {published data only}
    1. Villarruel G, Rubio DM, Lopez F, Cintioni J, Gurevech R, Romero G, et al. Saccharomyces boulardii in acute childhood diarrhea: a randomised placebo controlled study. Acta Paediatrica 2007;96(4):538-41. - PubMed
Vivatvakin 2006 {published data only}
    1. Vivatvakin B, Kowitdamrong E. Randomized control trial of live Lactobacillus acidophilus plus Bifidobacterium infantis in treatment of infantile acute watery diarrhea. Journal of the Medical Association of Thailand 2006;89:Suppl 3:S126-33. - PubMed
Wunderlich 1989 {published data only}
    1. Wunderlich PF, Braun L, Fumagalli I, D'Apuzzo V, Heim F, Karly M, et al. Double-blind report of the efficacy of lactic acid-producing Enterococcus SF68 in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoea. Journal of International Medical Research 1989;17(4):333-8. - PubMed
Xie 2013 {published data only}
    1. Xie YM, Gao S, Wang LY, Wang ZL. Therapeutic effect of probiotics and oral IgY as supplementary drugs in the treatment of pediatric rotavirus enteritis: a comparative study. Chinese Journal of Contemporary Pediatrics 2013;15(11):1000-5. - PubMed

References to studies excluded from this review

Agarwal 2001 {published data only}
    1. Agarwal KN, Bhasin SK, Faridi MMA, Mathur M, Gupta S. Lactobacillus casei in the control of acute diarrhoea - a pilot study. Indian Pediatrics 2001;38(8):905-10. - PubMed
Agarwal 2002 {published data only}
    1. Agarwal KN, Bhasin SK. Feasibility studies to control acute diarrhoea in children by feeding fermented milk preparations Actimel and Indian Dahi. European Journal of Clinical Nutrition 2002;56(Suppl. 4):S56-9. - PubMed
Ahmadipour 2018 {published data only (unpublished sought but not used)}
    1. Ahmadipour S, Motamed F, Mohsenzadeh A, Esfandiarpour B. Probiotic or zinc, which is more effective in treatment of diarrhea in children? Journal of Pediatric Gastroenterology and Nutrition Conference: 51st Annual Meeting European Society for Paediatric Gastroenterology, Hepatology and Nutrition 2018;66:332.
Alexander 1971 {published data only}
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Alvisi 1982 {published data only}
    1. Alvisi V, Tralli M, Loponte A, Pavani F, Massari M. Double-blind study of treatment with SF 68 or with antibiotics in acute enteritis in adults [Studio in doppio cieco sul trattamento con SF68 o con antibiotici nelle enteritis acute dell'adulto]. La Clinica Terapeutica 1982;101(6):581-6. - PubMed
Asmat 2018 {published data only (unpublished sought but not used)}
    1. Asmat S, Shaukat F, Asmat R, Bakhat H, Asmat TM. Clinical efficacy comparison of Saccharomyces boulardii and lactic acid as probiotics in acute pediatric diarrhea. Journal of the College of Physicians and Surgeons - Pakistan 2018;28:214-7. - PubMed
Barone 2000 {published data only}
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Beck 1961 {published data only}
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Bellomo 1979 {published data only}
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Bellomo 1980 {published data only}
    1. Bellomo G, Mangiagle A, Nicastro L, Frigeria G. A controlled double-blind study of SF68 strain as a new biological preparation for the treatment of diarrhoea in pediatrics. Current Therapeutic Research: Clinical and Experimental 1980;28(6):927-35.
Bellomo 1982 {published data only}
    1. Bellomo G, Finocchiaro C, Frigerio G, Mangiagli A, Nicastro L. Controlled study of Enterococcus LAB strain SF68 in acute enteritis in children with concomitant respiratory infection [Studio controllato sull'enterococco L.A.B. ceppo SF 68 nelle enteriti acute del bambino concomitanti ad infezioni delle vie respiratorie]. Clinica Pediatrica 1982;64:219-27.
Bin Li Xie 1995 {published data only}
    1. Bin Li Xie. Controlled clinical trial of Lacteol Fort Sachet versus furazolidone or berberine in treatment of acute diarrhoea in children [Étude contrôlée du Lactéol Fort sachets versus furazolidone ou berbérine dans le traitement des diarrhées aiguës de l'enfant]. Annales de Pediatrie 1995;42(6):396-401.
Boulloche 1994 {published data only}
    1. Boulloche J, Mouterde O, Mallet E. Management of acute diarrhoea in infants and young children. Controlled study of the anti-diarrheal efficacy of killed L. acidophilus (LB strain) versus a placebo and a reference drug (loperamide). Annales de Pediatrie 1994;41(7):457-63.
Brewster 2004 {published data only}
    1. Brewster DR, Ritchie B, McNeil Y, Davidson G, Butler R. Efficacy of probiotic therapy in Aboriginal children with acute diarrheal disease. Journal of Pediatric Gastroenterology and Nutrition 2004;39:S404. - PubMed
Camarri 1981 {published data only}
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Cetina Sauri 1990 {published data only}
    1. Cetina-Sauri G, Basto GS. Therapeutic evaluation of children with acute diarrhea. Tribuna Medica 1990;81(3):141-4.
Chandra 2002 {published data only}
    1. Chandra RK. Effect of Lactobacillus on the incidence and severity of acute rotavirus diarrhoea in infants. A prospective placebo-controlled double-blind study. Nutrition Research 2002;22(1):65-9.
Chapoy 1985 {published data only}
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Chicoine 1973 {published data only}
    1. Chicoine L, Joncas JH. Use of lactic enzymes in non-bacterial gastroenteritis [Emploi des ferments lactiques dans la gastro-entérite non bactérienne]. L'Union Médicale du Canada 1973;102(5):1114-5. - PubMed
Costa‐Ribeiro 2000a {published data only}
    1. Costa-Ribeiro H, Ribeiro TCM, Mattos AP, Almeida PS, Valois SS, Vanderhoof JA. Use of Lactobacillus GG in the treatment of severe, acute diarrhoea in adverse environmental conditions. Journal of Pediatric Gastroenterology and Nutrition 2000;31 Suppl 2:251-2.
Costa‐Ribeiro 2000b {published data only}
    1. Costa-Ribeiro H, Ribeiro TCM, Mattos AP, Lins EV, Neri DA, Valois SS, Vanderhoof JA. Prophylactic administration of Lactobacillus GG to children in a daycare center. Journal of Pediatric Gastroenterology and Nutrition 2000;31 Suppl 2:252.
Cui 2004 {published data only}
    1. Cui Y-L, Wan F-C, Tang D-L, Wu S-H. Efficacy of Bacillus coagulans tablets in the treatment of acute and chronic diarrhoea. International Journal of Immunotherapy 2004;20(1):17-22.
Czerwionka 2009 {published data only}
    1. Czerwionka-Szaflarska M, Murawska S, Swincow G. Evaluation of influence of oral treatment with probiotic and/or oral rehydration solution on course of acute diarrhoea in children. Przeglad Gastroenterologiczny 2009;4(3):166-72.
Dash 2016 {published data only}
    1. Dash DK, Dash M, Mohanty MD, Acharya N. Efficacy of probiotic Saccharomyces boulardii as an adjuvant therapy in acute childhood diarrhoea. Journal of Nepal Paediatric Society 2016;36(3):250-5.
de dios Pozo‐O 1978 {published data only}
    1. dios Pozo-Olano J, Warram JH Jr, Gomez RG, Cavazos MG. Effect of a lactobacilli preparation on traveler's diarrhoea. A randomised, double blind clinical trial. Gastroenterology 1978;74(5 Pt 1):829-30. - PubMed
Eren 2010 {published data only}
    1. Eren M, Dinleyici EC, Vandenplas Y. Clinical efficacy comparison of Saccharomyces boulardii and yogurt fluid in acute non-bloody diarrhea in children: a randomized, controlled, open label study. American Journal of Tropical Hygiene 2010;82(3):488-91. - PMC - PubMed
Escribano 2018 {published data only (unpublished sought but not used)}
    1. Escribano J, Ferre N, Gispert-Llaurado M, Luque V, Rubio-Torrents C, Zaragoza-Jordana M, et al. Bifidobacterium longum subsp infantis CECT7210-supplemented formula reduces diarrhea in healthy infants: a randomized controlled trial. Pediatric Research 2018;83:1120-8. - PubMed
Fang 2009 {published data only}
    1. Fang SB, Lee H-C, Hu J-J, Hou S-Y, Liu H-L, Fang H-W. Dose-dependent effect of Lactobacillus rhamnosus on quantitative reduction of faecal rotavirus shedding in children. Journal of Tropical Pediatrics 2009;55(5):297-301. - PubMed
Fourrier 1968 {published data only}
    1. Fourrier A, Lequien P. The treatment of infantile gastroenteritis by the use solely of a combination of colibacillus and lactobacillus. Apropos of 56 cases. Annales de Pediatrie 1968;15:491-5. - PubMed
Freedman 2018b {published data only}
    1. Freedman S, Williamson-Urquharta S, Farionb K, Gouinc S, Willand A, Poonaie N, et al. "Probiotics in acute gastroenteritis-benefit or harm?: a multicenter, randomized, double-blind, placebo-controlled clinical trial" in North American Congress of Clinical Toxicology (NACCT) Abstracts 2018. Clinical Toxicology 2018;56(10):912-1092. - PubMed
Frigerio 1986 {published data only}
    1. Frigerio G. A lactic acid producer enterococcus in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoeal disorders: a double-blind multicentre placebo-controlled clinical trial (Abstract). Digestive Diseases and Sciences 1986;31 Suppl:496.
Girola 1995 {published data only}
    1. Girola M, Ventura P. Efficacy of probiotic preparation with living, freeze-dried lactic acid bacteria and yeast on child diarrhoea [Efficacia di un prodotto probiotico a base di fermenti lattici e lievito vitali liofilizzati nel trattamento della diarrea del bambino]. Archivio di Medicina Interna 1995;47(2-3):61-72.
Gracheva 1996 {published data only}
    1. Gracheva NM, Gavrilov AF, Solov'eva AI, Smirnov VV, Sorokulova IB, Reznik SR, et al. The efficacy of the new bacterial preparation biosporin in treating acute intestinal infections. Zhurnal Mikrobiologii, Epidemiologii, i Immunobiologii 1996;1(1):75-7. - PubMed
Grandi 2009 {published data only}
    1. Grandi G, Medina M, Soria R, Teran C, Araya M. Probiotics in the management of acute rotavirus diarrhea in Bolivian children: a randomized, double-blind, controlled trial of two different preparations. In: Pediatric Research. Vol. 67. 2010:447 (abstract 10). - PMC - PubMed
Grandy 2010 {published data only}
    1. Grandy G, Medina M, Soria R, Terán CG, Araya M. Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infectious Diseases 2010;10:253. - PMC - PubMed
Hafeez 2002 {published data only}
    1. Hafeez A, Tariq P, Ali S, Kundi ZU, Khan A, Hassan M. The efficacy of Saccharomyces boulardii in the treatment of acute watery diarrhoea in children: a multicentre randomized controlled trial. Journal of College of Physicians and Surgeons Pakistan 2002;12(7):432-4.
Henker 2007b {published data only}
    1. Henker J, Blokhin BM, Bolbot YK, Maydannik VG. Acute diarrhoea in infants and small children. Successful adjuvant therapy with the probiotic Mutaflor [Akute diarrhő bei säuglingen und kleinkindern. Erfolgreiche adjuvante therapie mit dem probiotikum Mutaflor]. Pädiat. Prax 2007;71:605-10.
Heydarian 2010 {published data only}
    1. Heydarian F, Kianifar HR, Ahanchian H, Khakshure A, Seyedi J, Moshirian D. A comparison between traditional yogurt and probiotic yogurt in non-inflammatory acute gastroenteritis. Saudi Medical Journal 2010;31(3):280-3. - PubMed
Htwe 2008 {published data only}
    1. Htwe K, Yee KS, Tin M, Vandenplas Y. Effect of Saccharomyces boulardii in the treatment of acute watery diarrhea in Myanmar children: a randomized control study. American Journal of Tropical Medicine and Hygiene 2008;78(2):214-6. - PubMed
Isolauri 1991 {published data only}
    1. Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T. A human Lactobacillus strain (Lactobacillus casei GG) promotes recovery from acute diarrhea in children. Pediatrics 1991;88(1):90-7. - PubMed
Jimenez‐Rodriguez 2018 {published data only}
    1. Jimenez-Rodriguez C, Jimenez-Diaz J, Hernandez-Martinez F, Rodriguez-De-vera B. Efficacy of probiotics against acute diarrhoea in warm areas. In: Annals of Nutrition and Metabolism Conference: 9th workshop probiotics and prebiotics. Vol. 72. 2018.
Kaila 1992 {published data only}
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Khan 2012 {published data only}
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Khoshdel 2018 {published data only}
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Korviakova 2000 {published data only}
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Lahiri 2015a {published data only}
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Lahiri 2015b {published data only}
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Lei 2006 {published data only}
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Lievin Le‐Maol 2007 {published data only}
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Michielutti 1995 {published data only}
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Misra 2009 {published data only}
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Moraes 2001 {published data only}
    1. Moraes E, Chinzon D, Coelho LG, Fernandes TF, Haddad MT, et al. A multicentric, randomised, investigator-blind, parallel group study to assess the efficacy, safety and tolerability of Racecadotril versus Saccharomyces boulardii in the treatment of acute diarrhoea in adults [Estudo multicêntrico de grupos paralelos, randomizado, cego para o investigador, para avaliar a eficácia, segurança e tolerabilidade do racecadotril versus Saccharomyces boulardii no tratamento da diarréia aguda em adultos]. Revista Brasileira de Medicina 2001;58(1-2):65-74.
Niv 1963 {published data only}
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Perez 2019 {published data only}
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Pernica 2017 {published data only}
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Rautanen 1998 {published data only}
    1. Rautanen T, Isolauri E, Salo E, Vesikari T. Management of acute diarrhoea with low osmolarity oral rehydration solutions and Lactobacillus strain GG. Archives of Disease in Childhood 1998;79(2):157-60. - PMC - PubMed
Saint‐Marc 1991 {published data only}
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Satoh 1984 {published data only}
    1. Satoh Y, Iwata S, Iwata Y, Yamashita N, Oikawa T, Osano M, et al. Effect of Bifidobacterium breve administration on clinical course and intestinal flora in children with acute diarrhea [Abstract]. Nippon Shonikagakkai Zasshi 1984;88:2178-9.
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    1. Sindhu KNC, Sowmyanarayanan TV, Paul A, Babji S, Ajjampur SSR, Priyadarshini S, et al. Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clinical Infectious Diseases 2014;58(8):1107–15. - PMC - PubMed
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    1. Táborská J, Pazdiora P. Smecta and Lactobacillus acidophilus ND in the treatment of acute diarrhoea in children [Smecta a Lactobacillus acidophilus ND v lécbe akutních detských prujmu]. Ceskoslovenská Pediatrie 1997;52(1):29-33.
Tojo 1987 {published data only}
    1. Tojo M, Oikawa T, Morikawa Y, Yamashita N, Iwata S, Satoh Y, et al. The effects of Bifidobacterium breve administration on Campylobacter enteritis. Acta Paediatrica Japonica 1987;29(1):160-7. - PubMed
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References to ongoing studies

CTRI/2017/08/009543 {published data only}
    1. CTRI/2017/08/009543. Effect of probiotic Bacillus clausii UBBC07 in children with Acute Diarrhoea.http://ctri.nic.in/Clinicaltrials/advsearch.php 29 August 2017.
CTRI/2018/04/013360 {published data only}
    1. CTRI/2018/04/013360. Efficacy of Lactobacillus sporogenes in treating acute diarrhoea in adults-randomised control study.http://ctri.nic.in/Clinicaltrials/advsearch.php 19 April 2018.
CTRI/2018/06/014480 {published data only}
    1. CTRI/2018/06/014480. A multicentric, randomized, double blind, placebo controlled trial to assess the efficacy and safety of Saccharomyces boulardii CNCM-I 3799 Bacillus subtilis CU – 1 combination for treatment of acute diarrhoea in Indian children.http://ctri.nic.in/Clinicaltrials/advsearch.php 6 August 2018.
IRCT2017010312437N2 {published data only}
    1. IRCT2017010312437N2. Evaluation of the effect of ORS with probiotics, zinc and vitamin A on diarrhea in children, a double blind clinical trial.https://en.irct.ir/trial/12487 17 August 2017.
IRCT2017090812897N3 {published data only}
    1. IRCT2017090812897N3. The effect of yeast probiotic (Saccharomyces boulardii) on acute diarrhea in children.https://en.irct.ir/trial/12898 7 October 2017.
ISRCTN18444252 {published data only}ISRCTN
    1. ISRCTN18444252. Probiotics for treatment of acute childhood diarrhea.https://doi.org/10.1186/ISRCTN18444252 23 February 2018.
NCT03539913 {published data only}
    1. NCT03539913. Efficacy and Safety of Probiotics in the Treatment of Acute Gastroenteritis in Children (SABINA).https://clinicaltrials.gov/ct2/show/NCT03539913 30 May 2018.
NCT03684538 {published data only}
    1. NCT03684538. Efficacy of probiotics vs. zinc vs. probiotics-zinc combination on acute diarrhea in children.https://clinicaltrials.gov/ct2/show/NCT03684538 25 September 2018.

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