Probiotic use in at-risk populations
Open accessAbstract
OBJECTIVE: To inform health care providers about quality standards for manufacture of probiotic products being recommended for at-risk patient populations. SUMMARY: Probiotics are used in a variety of clinical settings, sometimes in at-risk populations for therapeutic endpoints. Although probiotics might not be approved as drugs, they are sometimes used for the prevention or treatment of disease. In the United States, and many regions of the world, probiotic products are marketed as dietary supplements (not drugs) and are therefore subject to different manufacturing and quality control standards than approved drugs are. Health care providers need to be assured that probiotic products used in at-risk populations are safe for this use. Pharmacists should require certificates of analysis, which document quality standards, from manufacturers of products stocked in hospital formularies or other pharmacies dispensing to at-risk people. Although responsible manufacturers use stringent quality standards on their processes and finished products, using a third party to verify compliance with manufacturing and accuracy of product labeling adds assurance to end users that the product is of high quality. CONCLUSION: It is in patients' best interest to use probiotics in the prevention and treatment of conditions when the evidence is convincing. To protect high-risk patients, probiotic products should meet stringent microbiological standards. Product testing results should be available for review before recommending probiotic products to at-risk individuals. For products used in at-risk populations, manufacturers should provide this information or participate in a third-party verification program that certifies compliance.
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There are two aspects to safety: establishing the adverse effect profile of specific single-strain and multi-strain supplements, and ensuring marketed supplements meet stringent quality standards to ensure correct strains are present and product is free of contamination.
“There are two aspects to safety: establishing the adverse effect profile of specific single-strain and multi-strain supplements (i.e., the safety of the strain(s) per se), and ensuring that marketed supplements meet stringent quality standards to ensure the correct strains are present and the product is free of contamination [217].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [217]
Probiotics have been studied in vulnerable groups including infants, patients with severe acute pancreatitis, inflammatory bowel diseases, liver diseases, HIV, and other conditions, with greater cause for concern for products containing high concentrations up to 450-900 billion live bacteria per dose.
“Further, probiotics have been studied in vulnerable groups, including infants, patients with severe acute pancreatitis, inflammatory bowel diseases, liver diseases, HIV, and other conditions [213, 216–218] with even greater cause for concern with the small number of products that contain high concentrations of up to 450–900 billion live bacteria per dose [211].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [217]
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Cites
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592 · see citing works
Besselink, M. G., van Santvoort, H. C., Buskens, E., Boermeester, M. A., van Goor, H., Timmerman, H. M., Nieuwenhuijs, V. B., Bollen, T. L., van Ramshorst, B., Witteman, B. J., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60207-x · Cited by 1,367 · see citing works
THE UNITED STATES PHARMACOPEIAL CONVENTION
Hirschfelder, A. D. (1930) · JAMA · doi:10.1001/jama.1930.02720030050030 · Cited by 1,015 · see citing works
Probiotics for prevention of necrotizing enterocolitis in preterm infants
AlFaleh, K. M., & Anabrees, J. (2014) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005496.pub4 · Cited by 965 · see citing works
Safety assessment of probiotics for human use
Sanders, M. E., Akkermans, L. M. A., Haller, D., Hammerman, C., Heimbach, J. T., Hörmannsperger, G., & Huys, G. (2010) · Gut Microbes · doi:10.4161/gmic.1.3.12127 · Cited by 816 · see citing works
Self-citationProbiotic use in clinical practice: what are the risks?
Boyle, R. J., Robins-Browne, R. M., & Tang, M. L. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.6.1256 · Cited by 776 · see citing works
Food fermentations: Microorganisms with technological beneficial use
Bourdichon, F., Casarégola, S., Farrokh, C., Frisvad, J. C., Gerds, M. L., Hammes, W. P., Harnett, J., Huys, G. R. B., Laulund, S., Ouwehand, A. C., et al. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.12.030 · Cited by 742 · see citing works
Self-citationEmergency Department Visits for Adverse Events Related to Dietary Supplements
Geller, A. I., Shehab, N., Weidle, N. J., Lovegrove, M. C., Wolpert, B. J., Timbo, B. B., Mozersky, R. P., & Budnitz, D. S. (2015) · New England Journal of Medicine · doi:10.1056/nejmsa1504267 · Cited by 502 · see citing works
(BIOHAZ), E. P. O. B. H., Koutsoumanis, K., Allende, A., Álvarez‐Ordóñez, A., Bolton, D., Bover‐Cid, S., Chemaly, M., Davies, R., Cesare, A. D., Hilbert, F., et al. (2021) · EFSA Journal · doi:10.2903/j.efsa.2021.6377 · Cited by 443 · see citing works
Davis, C. (2014) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2014.04.012 · Cited by 377 · see citing works
Host-microbial interactions in the metabolism of therapeutic and diet-derived xenobiotics
Carmody, R. N., & Turnbaugh, P. J. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72335 · Cited by 268 · see citing works
Safety of probiotics used to reduce risk and prevent or treat disease.
(2011) · PubMed Central · Cited by 242 · see citing works
Lee, J., Chu, S. H., Jeon, J. Y., Lee, M. K., Park, J., Lee, D., Lee, J., & Kim, N. K. (2014) · Digestive and Liver Disease · doi:10.1016/j.dld.2014.09.004 · Cited by 136 · see citing works
Villar-García, J., Hernández, J. J., Güerri‐Fernández, R., González, A., Lerma, E., Guelar, A., Saenz, D. C., Sorlí, L., Montero, M., Horcajada, J. P., et al. (2014) · JAIDS Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/qai.0000000000000468 · Cited by 124 · see citing works
Meini, S., Laureano, R., Fani, L., Tascini, C., Galano, A., Antonelli, A., & Rossolini, G. M. (2015) · Infection · doi:10.1007/s15010-015-0798-2 · Cited by 106 · see citing works
Mattia, A., & Merker, R. I. (2008) · Clinical Infectious Diseases · doi:10.1086/523329 · Cited by 86 · see citing works
Safety of probiotics and synbiotics in children under 18 years of age
van den Nieuwboer, M., Brummer, R. J., Guarner, F., Morelli, L., Cabana, M., & Claassen, E. (2015) · Beneficial Microbes · doi:10.3920/bm2014.0157 · Cited by 83 · see citing works
Self-citationProbiotic and synbiotic safety in infants under two years of age
van den Nieuwboer, M., Claassen, E., Morelli, L., Guarner, F., & Brummer, R. J. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0046 · Cited by 78 · see citing works
(BIOHAZ), E. P. O. B. H. (2015) · EFSA Journal · doi:10.2903/j.efsa.2015.4138 · Cited by 73 · see citing works
Micronutrient supplemented probiotic yogurt for HIV-infected adults taking HAART in London, Canada
Hemsworth, J., Hekmat, S., & Reid, G. (2012) · Gut Microbes · doi:10.4161/gmic.21248 · Cited by 66 · see citing works
Self-citationPrevalence of probiotic use among inpatients: A descriptive study of 145 U.S. hospitals
Yi, S. H., Jernigan, J. A., & McDonald, L. C. (2016) · American Journal of Infection Control · doi:10.1016/j.ajic.2015.12.001 · Cited by 52 · see citing works
Cochrane in context: Probiotics for prevention of necrotizing enterocolitis in preterm infants
Robinson, J. L. (2014) · Evidence-Based Child Health A Cochrane Review Journal · doi:10.1002/ebch.1977 · Cited by 34 · see citing works
Bacterial counts from five over-the-counter probiotics: Are you getting what you paid for?
Goldstein, E. J. C., Citron, D. M., Claros, M. C., & Tyrrell, K. L. (2013) · Anaerobe · doi:10.1016/j.anaerobe.2013.10.005 · Cited by 31 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Hill C, Guarner F, Reid G, et al. Expert consensus document. The Inter- national Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506e514.
- Gregory Leyer, PhD, Chief Scientific Officer, UAS Laboratories, Madison, WI M.E. Sanders et al. / Journal of the American Pharmacists Association 56 (2016) 680e686
Cited by
Sorted by citations
Swanson, K. S., Gibson, G. R., Hutkins, R., Reimer, R. A., Reid, G., Verbeke, K., Scott, K. P., Holscher, H. D., Azad, M. B., Delzenne, N. M., et al. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0344-2 · Cited by 2,196 · see citing works
Self-citationHealth Benefits of Heat-Killed (Tyndallized) Probiotics: An Overview
Piqué, N., Berlanga, M., & Miñana-Galbis, D. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102534 · Cited by 642 · see citing works
Emerging issues in probiotic safety: 2023 perspectives
Merenstein, D., Pot, B., Leyer, G., Ouwehand, A. C., Preidis, G. A., Elkins, C. A., Hill, C., Lewis, Z. T., Shane, A. L., Zmora, N., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2185034 · Cited by 481 · see citing works
Self-citationThe Unregulated Probiotic Market
de Simone, C. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.01.018 · Cited by 317 · see citing works
Sanders, M. E., Merenstein, D., Merrifield, C. A., & Hutkins, R. (2018) · Nutrition Bulletin · doi:10.1111/nbu.12334 · Cited by 278 · see citing works
Self-citationInternational Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · see citing works
Using Probiotics to Flatten the Curve of Coronavirus Disease COVID-2019 Pandemic
Baud, D., Dimopoulou Agri, V., Gibson, G. R., Reid, G., & Giannoni, E. (2020) · Frontiers in Public Health · doi:10.3389/fpubh.2020.00186 · Cited by 240 · see citing works
Self-citationKolaček, S., Hojsak, I., Berni Canani, R., Guarino, A., Indrio, F., Orel, R., Pot, B., Shamir, R., Szajewska, H., Vandenplas, Y., et al. (2017) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001603 · Cited by 224 · see citing works
World Gastroenterology Organisation Global Guidelines: Probiotics and Prebiotics
Guarner, F., Sanders, M. E., Szajewska, H., Cohen, H., Eliakim, R., Herrera-deGuise, C., Karakan, T., Merenstein, D., Piscoya, A., Ramakrishna, B., et al. (2024) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000002002 · Cited by 209 · see citing works
Self-citationImproving End-User Trust in the Quality of Commercial Probiotic Products
Jackson, S. A., Schoeni, J. L., Vegge, C., Pane, M., Stahl, B., Bradley, M., Goldman, V. S., Burguière, P., Atwater, J. B., & Sanders, M. E. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00739 · Cited by 192 · see citing works
Self-citationConsiderations for determining safety of probiotics: A USP perspective
Roe, A. L., Boyte, M.-E., Elkins, C. A., Goldman, V. S., Heimbach, J., Madden, E., Oketch-Rabah, H., Sanders, M. E., Sirois, J., & Smith, A. (2022) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2022.105266 · Cited by 136 · see citing works
Self-citationSpacova, I., Binda, S., ter Haar, J. A., Henoud, S., Legrain-Raspaud, S., Dekker, J., Espadaler-Mazo, J., Langella, P., Martín, R., Pane, M., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1272754 · Cited by 129 · see citing works
Self-citationda Silva, T. F., Glória, R. D. A., Americo, M. F., Freitas, A. D. S., de Jesus, L. C. L., Barroso, F. A. L., Laguna, J. G., Coelho-Rocha, N. D., Tavares, L. M., le Loir, Y., et al. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-024-10247-x · Cited by 117 · see citing works
Zorzela, L., Ardestani, S. K., McFarland, L. V., & Vohra, S. (2017) · Beneficial Microbes · doi:10.3920/bm2017.0032 · Cited by 44 · see citing works
- Authors
- Sanders, M. E., Merenstein, D. J., Ouwehand, A. C., Reid, G., Salminen, S., Cabana, M. D., Paraskevakos, G., & Leyer, G.
- Corresponding author
- Sanders, Mary Ellen
- ORCID
- Venue
- Journal of the American Pharmacists Association
- Publisher
- Elsevier BV
- Published
- 2016-11
- Volume
- 56
- Issue
- 6
- Pages
- 680-686
- ISSN
- 1544-3191 (ISSN-L)
- OpenAlex
- W2549916053
- Cited by
- 129
- References
- 24
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 17 · 2023: 16 · 2022: 9 · 2021: 12 · 2020: 14 · 2019: 14 · 2018: 17 · 2017: 5 · 2016: 1
- FWCI
- 15.54
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of the American Pharmacists Association (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Scholarship@Western (Western University) (submittedVersion)
- Funders
- United States Pharmacopeia
- U.S. Food and Drug Administration
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Complementary and alternative medicine › Complementary and Alternative Medicine Studies
- Health Sciences › Health Professions › Health Information Management › Healthcare Regulation
- Keywords
- probiotics, vulnerable populations, probiotic quality control, production standards, dietary supplements, microbiological standards, third-party verification, product labeling, hospital formulary, pharmacist recommendations, probiotic safety
- MeSH terms
- Food Labeling, Humans, Pharmacists, Quality Control, Risk Factors, United States, Dietary Supplements, Food Industry, Probiotics, Professional Role
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