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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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Sanders, M. E., Goh, Y. J., & Klaenhammer, T. R. (2019) · ASM Press eBooks · doi:10.1128/9781555819972.ch32 · Cited by 32
Koon, H. W., Su, B., Xu, C., Mussatto, C. C., Tran, D. H.-N., Lee, E. C., ORTIZ, C. W., Wang, J., Lee, J. E., Ho, S., et al. (2016) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00150.2016 · Cited by 32
Characterisation and therapeutic manipulation of the gut microbiome in inflammatory bowel disease
Schulberg, J. D., & Cruz, P. P. D. (2016) · Internal Medicine Journal · doi:10.1111/imj.13003 · Cited by 32
Sinclair, A., Xie, X., Saab, L., & Dendukuri, N. (2016) · CMAJ Open · doi:10.9778/cmajo.20160087 · Cited by 31
van Wietmarschen, H., Busch, M., van Oostveen, A., Pot, G. K., & Jong, M. C. (2020) · BMC Gastroenterology · doi:10.1186/s12876-020-01297-w · Cited by 33
“No serious adverse events have been found to be attributed to probiotics, and the risk for adverse events has been similar to that of control groups [8, 9].”
BackgroundA novel probiotic therapeutic in a murine model of Clostridioides difficile colitis
Shelby, R. D., Janzow, G. E., Mashburn‐Warren, L., Galley, J. D., Tengberg, N., Navarro, J. B., Conces, M. R., Bailey, M. T., Goodman, S. D., & Besner, G. E. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1814119 · Cited by 31
“Furthermore, in all of these studies, probiotics were administered in their planktonic state and required repeated doses to demonstrate efficacy.(28,29) In the current study, we have demonstrated that the administration of one single dose of Lr in its biofilm state can significantly reduce the incidence and severity o…”
ResultBifidobacteria and Their Health-Promoting Effects
Hidalgo-Cantabrana, C., Delgado, S., Ruíz, L., Ruas‐Madiedo, P., Sánchez, B., & Margollés, A. (2018) · ASM Press eBooks · doi:10.1128/9781555819705.ch3 · Cited by 32
Bugs or drugs: Are probiotics safe for use in the critically ill?
Urben, L. M., Wiedmar, J., Boettcher, E., Cavallazzi, R., Martindale, R. G., & McClave, S. A. (2014) · Current Gastroenterology Reports · doi:10.1007/s11894-014-0388-y · Cited by 29
Nagarajan, A., Scoggin, K., Gupta, J., Threadgill, D. W., & Andrews‐Polymenis, H. L. (2023) · Microbiome · doi:10.1186/s40168-023-01552-8 · Cited by 30
Use of probiotics in prevention and treatment of patients with Clostridium difficile infection
Ollech, J. E., Shen, N. T., Crawford, C. V., & Ringel, Y. (2016) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2016.01.002 · Cited by 30
Gaisawat, M. B., MacPherson, C. W., Tremblay, J., Piano, A., Iskandar, M. M., Tompkins, T. A., & Kubow, S. J. (2019) · Microorganisms · doi:10.3390/microorganisms8010060 · Cited by 30
Recurrent Clostridioides difficile infection: Recognition, management, prevention
Tsigrelis, C. (2020) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.87gr.20001 · Cited by 30
van Werkhoven, C. H., van der Tempel, J., Jajou, R., Thijsen, S. F. T., Diepersloot, R. J. A., Bonten, M. J. M., Postma, D. F., & Oosterheert, J. J. (2015) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2015.04.005 · Cited by 30
Maione, A., Imparato, M., Buonanno, A., Salvatore, M. M., Carraturo, F., de Alteriis, E., Guida, M., & Galdiero, E. (2024) · Foods · doi:10.3390/foods13071013 · Cited by 32
Probiotics in Newborns and Children
Lenfestey, M. W., & Neu, J. (2017) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2017.08.006 · Cited by 29
Doll, M. E., Marra, A. R., Apisarnthanarak, A., Al-Maani, A. S., Abbas, S. M., & Rosenthal, V. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.10.039 · Cited by 29
Ladizinski, B., McLean, R., Lee, K. C., Elpern, D. J., & Eron, L. J. (2014) · International Journal of Dermatology · doi:10.1111/ijd.12609 · Cited by 28
Differences of the Fecal Microflora With Clostridium difficile Therapies
Louie, T., Byrne, B., Emery, J. C. H., Ward, L., Krulicki, W., Nguyen, D., Wu, K., & Cannon, K. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ252 · Cited by 28
“A consensus is emerging that probiotics may be of benefit in preventing CDI [10].”
BackgroundThe Potential of Probiotics to Prevent Clostridium difficile Infection
Allen, S. J. (2015) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2014.11.002 · Cited by 28
Targeting Microbiota: What Do We Know about It at Present?
Derovs, A., Laivacuma, S., & Krūmiņa, A. (2019) · Medicina · doi:10.3390/medicina55080459 · Cited by 31
Hui, H., Wu, Y., Zheng, T., Zhou, S., & Tan, Z. (2020) · Medical Science Monitor · doi:10.12659/msm.921771 · Cited by 28
How to: prophylactic interventions for prevention of Clostridioides difficile infection
Reigadas, E., van Prehn, J., Falcone, M., Fitzpatrick, F., Vehreschild, M. J. G. T., Kuijper, E. J., & Bouza, E. (2021) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2021.06.037 · Cited by 28
Bainum, T. B., Reveles, K. R., Hall, R. G., Cornell, K., & Álvarez, C. A. (2023) · Microorganisms · doi:10.3390/microorganisms11020387 · Cited by 29
Kwon, J. H., Bommarito, K. M., Reske, K. A., Seiler, S. M., Hink, T., Babcock, H. M., Kollef, M. H., Fraser, V. J., Burnham, C. D., & Dubberke, E. R. (2015) · Infection Control and Hospital Epidemiology · doi:10.1017/ice.2015.195 · Cited by 28
A Review of the Economics of Treating Clostridium difficile Infection
Mergenhagen, K. A., Wojciechowski, A. L., & Paladino, J. A. (2014) · PharmacoEconomics · doi:10.1007/s40273-014-0161-y · Cited by 27
Barnes, D. M., & Yeh, A. M. (2015) · Nutrition in Clinical Practice · doi:10.1177/0884533615610081 · Cited by 28
Effect of Lactobacillus plantarum Strains on Clinical Isolates of Clostridium difficile in vitro
Rätsep, M. (2014) · Journal of Probiotics & Health · doi:10.4172/2329-8901.1000119 · Cited by 27
Consenso mexicano sobre probióticos en gastroenterología
Valdovinos, M. A., Montijo, E., y Abreu, A. T. A., Heller, S., Garay, A. G. G., Nogales, D. B., Bielsa-Fernández, M. V., Bojórquez-Ramos, M. D. C., Bosques‐Padilla, F., Burguete-García, A. I., et al. (2017) · Revista de Gastroenterología de México · doi:10.1016/j.rgmx.2016.08.004 · Cited by 31
New horizons in hospital acquired pneumonia in older people
Ewan, V. C., Hellyer, T. P., Newton, J. L., & Simpson, J. A. (2017) · Age and Ageing · doi:10.1093/ageing/afx029 · Cited by 27
Carvour, M. L., Wilder, S., Ryan, K. L., Walraven, C. J., Qeadan, F., Brett, M., & Page, K. A. (2018) · American Journal of Infection Control · doi:10.1016/j.ajic.2018.07.014 · Cited by 27
Zielińska, D., Sionek, B., & Kołożyn-Krajewska, D. (2018) · Diet, Microbiome and Health · doi:10.1016/b978-0-12-811440-7.00006-5 · Cited by 34
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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