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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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“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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Kumagai, T., Rahman, F. Z., & Smith, A. M. (2018) · Nutrients · doi:10.3390/nu10101405 · Cited by 162
Goodman, C., Keating, G., Georgousopoulou, E., Hespe, C., & Levett, K. (2021) · BMJ Open · doi:10.1136/bmjopen-2020-043054 · Cited by 163
Reappraisal of probiotics’ safety in human
Sotoudegan, F., Daniali, M., Hassani, S., Nikfar, S., & Abdollahi, M. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.04.032 · Cited by 154
van Hemert, S., Breedveld, A. C., Rovers, J. M. P., Vermeiden, J. P. W., Witteman, B. J. M., Smits, M. G., & de Roos, N. M. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00241 · Cited by 150
A prospective longitudinal study on the microbiota composition in amyotrophic lateral sclerosis
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
Probiotics and gastrointestinal conditions: An overview of evidence from the Cochrane Collaboration
Parker, E. A. D., Roy, T., D’Adamo, C. R., & Wieland, L. S. (2017) · Nutrition · doi:10.1016/j.nut.2017.06.024 · Cited by 152
Breakthroughs in the treatment and prevention of Clostridium difficile infection
Kociolek, L. K., & Gerding, D. N. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.220 · Cited by 156
Mantegazza, C., Molinari, P., D’Auria, E., Sonnino, M., Morelli, L., & Zuccotti, G. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.08.001 · Cited by 149
Healthcare-Associated Infections
Coffin, S. E., & Zaoutis, T. E. (2008) · Elsevier eBooks · doi:10.1016/b978-0-7020-3468-8.50107-3 · Cited by 146
S2k-Leitlinie Gastrointestinale Infektionen und Morbus Whipple
Autoren:, & Affiliation:, W. M. D. L. I. A. R. E. (2015) · Zeitschrift für Gastroenterologie · doi:10.1055/s-0034-1399337 · Cited by 145
“[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 144
Safety of Probiotics: Functional Fruit Beverages and Nutraceuticals
Žuntar, I., Petrić, Z., Kovačević, D. B., & Putnik, P. (2020) · Foods · doi:10.3390/foods9070947 · Cited by 142
Critical Appraisal of Oral Pre- and Probiotics for Caries Prevention and Care
Zaura, E., & Twetman, S. (2019) · Caries Research · doi:10.1159/000499037 · Cited by 137
Vitetta, L., Vitetta, G., & Hall, S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02240 · Cited by 137
Clostridium difficile disease: Diagnosis, pathogenesis, and treatment update
Napolitano, L. M., & Edmiston, C. E. (2017) · Surgery · doi:10.1016/j.surg.2017.01.018 · Cited by 132
AGA Technical Review on the Role of Probiotics in the Management of Gastrointestinal Disorders
Preidis, G. A., Weizman, A. V., Kashyap, P., & Morgan, R. L. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.05.060 · Cited by 137
Current understanding of antibiotic-associated dysbiosis and approaches for its management
Kesavelu, D., & Jog, P. P. (2023) · Therapeutic Advances in Infectious Disease · doi:10.1177/20499361231154443 · Cited by 156
Let thy food be thy medicine….when possible
Witkamp, R. F., & van Norren, K. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.06.026 · Cited by 131
The role of gut microbiota in intestinal disease: from an oxidative stress perspective
Sun, Y., Wang, X., Li, L., Zhong, C., Zhang, Y., Yang, X., Li, M., & Yang, C. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1328324 · Cited by 141
Probiotics, prebiotics, and the host microbiome: the science of translation
Petschow, B., Doré, J., Hibberd, P., Dinan, T., Reid, G., Blaser, M., Cani, P. D., Degnan, F. H., Foster, J., Gibson, G., et al. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12303 · Cited by 124
A successful history: probiotics and their potential as antimicrobials
Santacroce, L., Charitos, I. A., & Bottalico, L. (2019) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2019.1645597 · Cited by 129
“rhamnosus, administered at a high dose (10–50 billion CFUs per day) [154,155].”
BackgroundShould There Be a Recommended Daily Intake of Microbes?
Marco, M. L., Hill, C., Hutkins, R. W., Slavin, J. L., Tancredi, D. J., Merenstein, D. J., & Sanders, M. E. (2020) · Journal of Nutrition · doi:10.1093/jn/nxaa323 · Cited by 121
Wall, S. (2019) · Global Health Action · doi:10.1080/16549716.2020.1756191 · Cited by 120
Trubiano, J. A., Cheng, A. C., Korman, T. M., Röder, C., Campbell, A. J., May, M., Blyth, C. C., Ferguson, J., Blackmore, T., Riley, T. V., et al. (2016) · Internal Medicine Journal · doi:10.1111/imj.13027 · Cited by 119
Prebiotics and Probiotics for Gastrointestinal Disorders
Rau, S., Gregg, A., Yaceczko, S. D., & Limketkai, B. N. (2024) · Nutrients · doi:10.3390/nu16060778 · Cited by 127
Antiamoebic drugs for treating amoebic colitis
Gonzales, M. L. M., Dans, L. F., & Martinez, E. G. (2009) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006085.pub2 · Cited by 110
Health Professionals’ Knowledge of Probiotics: An International Survey
Fijan, S., Frauwallner, A., Varga, L., Langerholc, T., Rogelj, I., Lorber, M., Lewis, P., & Povalej, P. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16173128 · Cited by 110
“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).”
BackgroundInfluentialMcFarland, L. (2015) · Antibiotics · doi:10.3390/antibiotics4020160 · Cited by 109
Clostridium difficile infection: molecular pathogenesis and novel therapeutics
Rineh, A., Kelso, M. J., Vatansever, F., Tegos, G. P., & Hamblin, M. R. (2014) · Expert Review of Anti-infective Therapy · doi:10.1586/14787210.2014.866515 · Cited by 120
Wei, D., Heus, P., van de Wetering, F. T., van Tienhoven, G., Verleye, L., & Scholten, R. J. P. M. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd008831.pub3 · Cited by 108
“…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
Kociolek, L. K., Gerding, D. N., Carrico, R., Carling, P., Donskey, C. J., Dumyati, G. K., Kuhar, D. T., Loo, V. G., Maragakis, L. L., Pogorzelska‐Maziarz, M., et al. (2023) · Infection Control and Hospital Epidemiology · doi:10.1017/ice.2023.18 · Cited by 112
A randomized controlled trial of probiotics for Clostridium difficile infection in adults (PICO)
Barker, A., Duster, M. N., Valentine, S., Hess, T., Archbald‐Pannone, L. R., Guerrant, R. L., & Safdar, N. (2017) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkx254 · Cited by 106
Jump, R., Crnich, C. J., Mody, L., Bradley, S., Nicolle, L. E., & Yoshikawa, T. T. (2018) · Journal of the American Geriatrics Society · doi:10.1111/jgs.15248 · Cited by 104
Metadata
- 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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