Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children
Open accessAbstract
BACKGROUND: Antibiotics are widely prescribed; however they can cause disturbances in gastrointestinal flora which may lead to reduced resistance to pathogens such as Clostridium difficile (C. difficile). Probiotics are live organisms thought to balance the gastrointestinal flora. OBJECTIVES: The primary objectives were to assess the efficacy and safety of probiotics for preventing Clostridium difficile-associated diarrhea (CDAD) or C. difficile infection in adults and children. SEARCH METHODS: On February 21, 2013 we searched PubMed (1966-2013), EMBASE (1966-2013), Cochrane Central Register of Controlled Trials (The Cochrane Library 2013, Issue 1), CINAHL (1982-2013), AMED (1985-2013), and ISI Web of Science. Additionally, we conducted an extensive grey literature search including contact with industry representatives. SELECTION CRITERIA: Randomized controlled (placebo, alternative prophylaxis, or no treatment control) trials investigating probiotics (any strain, any dose) for prevention of CDAD, or C. difficile infection were considered for inclusion. DATA COLLECTION AND ANALYSIS: Two authors independently and in duplicate extracted data and assessed risk of bias using pre-constructed, and piloted, data extraction forms. Any disagreements were resolved by a third adjudicator. For articles published in abstract form only, further information was sought by contacting principal authors. The primary outcome was the incidence of CDAD. Secondary outcomes included the incidence of C. difficile infection, adverse events, antibiotic-associated diarrhea (AAD) and length of hospital stay. Dichotomous outcomes (e.g. incidence of CDAD) were pooled using a random-effects model to calculate the relative risk and corresponding 95% confidence interval (95% CI). Continuous outcomes (e.g. length of hospital) were pooled using a random-effects model to calculate the mean difference and corresponding 95% CI. Sensitivity analyses were conducted to explore the impact of missing data on efficacy and safety outcomes. For the sensitivity analyses, we assumed that the event rate for those participants in the control group who had missing data was the same as the event rate for those participants in the control group who were successfully followed. For the probiotic group we calculated effects using the following assumed ratios of event rates in those with missing data in comparison to those successfully followed: 1.5:1, 2:1, 3:1, and 5:1. To explore possible explanations for heterogeneity, a priori subgroup analysis were conducted on probiotic species, dose, adult versus pediatric population, and risk of bias.The overall quality of the evidence supporting each outcome was assessed using the GRADE criteria. MAIN RESULTS: A total of 1871 studies were identified with 31 (4492 participants) meeting eligibility requirements for our review. Overall 11 studies were rated as a high risk of bias due mostly to missing outcome data. A complete case analysis (i.e. participants who completed the study) of those trials investigating CDAD (23 trials, 4213 participants) suggests that probiotics significantly reduce this risk by 64%. The incidence of CDAD was 2.0% in the probiotic group compared to 5.5% in the placebo or no treatment control group (RR 0.36; 95% CI 0.26 to 0.51). Sixteen of 23 trials had missing CDAD data ranging from 5% to 45%. These results proved robust to sensitivity analyses of plausible and worst-plausible assumptions regarding missing outcome data and were similar whether considering trials in adults versus children, lower versus higher doses, different probiotic species, or higher versus lower risk of bias. Our judgment is that the overall evidence warrants moderate confidence in this large relative risk reduction. We downgraded the overall quality of evidence for CDAD to 'moderate' due to imprecision. There were few events (154) and the calculated optimal information size (n = 8218) was more than the total sample size. With respect to the incidence of C. difficile infection, a secondary outcome, pooled complete case results from 13 trials (961 participants) did not show a statistically significant reduction. The incidence of C. difficile infection was 12.6% in the probiotics group compared to 12.7% in the placebo or no treatment control group (RR 0.89; 95% CI 0.64 to 1.24). Adverse events were assessed in 26 studies (3964 participants) and our pooled complete case analysis indicates probiotics reduce the risk of adverse events by 20% (RR 0.80; 95% CI 0.68 to 0.95). In both treatment and control groups the most common adverse events included abdominal cramping, nausea, fever, soft stools, flatulence, and taste disturbance. For the short-term use of probiotics in patients that are not immunocompromised or severely debilitated, we consider the strength of this evidence to be moderate. AUTHORS' CONCLUSIONS: Based on this systematic review and meta-analysis of 23 randomized controlled trials including 4213 patients, moderate qua
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There is moderate evidence from a meta-analysis of 23 clinical trials (n=4,213) that probiotics are effective in preventing Clostridium difficile-associated diarrhea.
“Goldenberg and coworkers (113) concluded, after an exhaustive meta-analysis (23 clinical trials, n = 4,213), that there is moderate evidence suggesting that probiotics are effective in the prevention of CDAD.”
From Bifidobacteria and Their Health-Promoting Effects (2017) · cites this paper as [113]
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Flagged first, then by citations
6 of the 173 references couldn’t be matched to a known paper.
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Sorted by citations
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592 · see citing works
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“…diarrhea (AAD) and H. pylori infection 135,136,137 , defecation frequency 138,139 , infantile colic, 140 , mild to moderate ulcerative colitis, 141 irritable bowel syndrome, 142 treatment of acute diarrhea 143 prevention of C. difficile -associated diarrhea 144 and neonatal sepsis.”
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“difficile, acting as both preventive and treatment; however, most of the studies mainly provided clinical effects and tolerance and safety data but did not provide potential mechanisms of action (16, 45, 47, 48).”
BackgroundFernandes, A. D., Reid, J. N., Macklaim, J. M., McMurrough, T. A., Edgell, D. R., & Gloor, G. B. (2014) · Microbiome · doi:10.1186/2049-2618-2-15 · Cited by 1,329 · see citing works
“Introduction The rapid expansion of microbiome [1-5] and probiotic [6-9] research over the past 10 years and the many spinoffs providing novel insights into human and animal diseases, as well as products designed to alleviate them, have been primarily driven by sizeable funding from developed countries, especially Can…”
BackgroundGut Microbiome: Profound Implications for Diet and Disease
Hills, R. D., Pontefract, B., Mishcon, H. R., Black, C. A., Sutton, S. C., & Theberge, C. R. (2019) · Nutrients · doi:10.3390/nu11071613 · Cited by 1,107 · see citing works
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“Two meta-analyses showed that the incidence of CDI is lower in adult patients who receive probiotics in addition to antibiotic treatment than in those who received placebo (Johnson et al., 2012; Goldenberg et al., 2013), while another meta-analysis produced similar findings in children (Goldenberg et al.”
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Clostridium difficile infection
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“An updated Cochrane review on the use of probiotics for prevention of CDI found that probiotics are effective in trials with a C. dif fi cile associated diarrhoea baseline risk of > 5% (NNTB ¼ 12; moderate certainty evidence) [257].”
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“The short-term administration of probiotics appeared to be safe and effective in combination with antibiotics in patients who were not immunocompromised or severely debilitated, thus concluding that vulnerable patients should be informed of the potential benefits and risks of probiotics [23].”
BackgroundACG Clinical Guidelines: Prevention, Diagnosis, and Treatment of Clostridioides difficile Infections
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How Probiotics Affect the Microbiota
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“difficile-associated diarrhea.(44) Novel C.”
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Lactobacilli and Bifidobacteria in Human Breast Milk
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Using Probiotics to Flatten the Curve of Coronavirus Disease COVID-2019 Pandemic
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World Gastroenterology Organisation Global Guidelines: Probiotics and Prebiotics
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Emerging Priorities for Microbiome Research
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“In addition, many reviews still fail to account for strain-specificity and pool different types of probiotics together in their analysis [280, 281, 284].”
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Di Gioia, D., Bozzi Cionci, N., Baffoni, L., Amoruso, A., Pane, M., Mogna, L., Gaggìa, F., Lucenti, M. A., Bersano, E., Cantello, R., et al. (2020) · BMC Medicine · doi:10.1186/s12916-020-01607-9 · Cited by 151 · see citing works
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“[194] Aufgrund der Heterogenität der untersuchten Probiotika wurde dennoch die Evidenz der Studien für einen präventiven Effekt als insgesamt nur moderat eingestuft.”
BackgroundClostridioides difficile Infection
Guh, A. Y., & Kutty, P. K. (2018) · Annals of Internal Medicine · doi:10.7326/aitc201810020 · Cited by 137 · see citing works
Safety of Probiotics: Functional Fruit Beverages and Nutraceuticals
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Critical Appraisal of Oral Pre- and Probiotics for Caries Prevention and Care
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AGA Technical Review on the Role of Probiotics in the Management of Gastrointestinal Disorders
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Let thy food be thy medicine….when possible
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Probiotics, prebiotics, and the host microbiome: the science of translation
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“rhamnosus, administered at a high dose (10–50 billion CFUs per day) [154,155].”
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Prebiotics and Probiotics for Gastrointestinal Disorders
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“The median score for the self-evaluation of the knowledge of probiotics was 3 (95% CI: [3,4]) in both sexes, so there was no statistical difference between male and female health professionals in this respect (U = 83263.0; p = 0.134).”
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Clostridium difficile infection: molecular pathogenesis and novel therapeutics
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“…that, based on moderate-certainty evidence, probiotics are both safe and eHective for prevention of Clostridium di icile-associated diarrhoea in adults and children but do not significantly reduce the incidence of C di icile infection compared with placebo or no treatment (Goldenberg 2013).”
BackgroundStrategies to prevent Clostridioides difficile infections in acute-care hospitals: 2022 Update
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A randomized controlled trial of probiotics for Clostridium difficile infection in adults (PICO)
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- Authors
- Goldenberg, J. Z., Ma, S. S., Saxton, J. D., Martzen, M. R., Vandvik, P. O., Thorlund, K., Guyatt, G. H., & Johnston, B. C.
- Affiliations
- Bastyr University (US)
- McMaster University; Division of Plastic & Reconstructive Surgery; 1200 Main Street West - HSC 4E9 Hamilton Ontario Canada L8N 3Z5
- Nasjonalt Kunnskapssenter for Helsetjenesten (NO)
- McMaster University (CA)
- University of Toronto (CA)
- Venue
- Cochrane Database of Systematic Reviews
- Publisher
- Wiley
- Published
- 2013-05-31
- Volume
- 12
- Issue
- 5
- Pages
- CD006095-CD006095
- ISSN
- 1361-6137 (ISSN-L)
- 1465-1858
- PMC
- PMC6486212
- OpenAlex
- W1505136191
- Cited by
- 741
- References
- 173
- Citations by year
- 2026: 1 · 2025: 12 · 2024: 42 · 2023: 60 · 2022: 54 · 2021: 74 · 2020: 79 · 2019: 85 · 2018: 80 · 2017: 65 · 2016: 54 · 2015: 59 · 2014: 51 · 2013: 20
- FWCI
- 7.92
- Type
- journal article
- Language
- en
- Update notices
- new_version (2017-12-19)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cochrane Database of Systematic Reviews (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UTS ePRESS (University of Technology Sydney) (submittedVersion)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotics, Clostridium difficile, Clostridium difficile-associated diarrhea, Clostridium difficile infection, antibiotic-associated diarrhea, antibiotic prophylaxis, gut microbiota, length of hospital stay, adverse events, children, adults, probiotic safety, probiotic efficacy, risk of bias, heterogeneity, subgroup analysis, risk of bias assessment
- MeSH terms
- Adult, Anti-Bacterial Agents, Child, Diarrhea, Enterocolitis, Pseudomembranous, Humans, Randomized Controlled Trials as Topic, Clostridioides difficile, Probiotics
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