Probiotics: Reiterating what they are and what they are not

Frontiers in Microbiology

Volumn 10, Issue MAR, 2019, Pages

  Reid, Gregor ^a,b   Gadir, Azza A ^c,d   Dhir, Raja ^e  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Seed Health Inc   (United States)

Author keywords

Human health; Human microbiome; Microbial therapies; Probiotics; Requirements; Scientific definition; Stewardship; Translational microbiology

Indexed keywords

CIPROFLOXACIN; METRONIDAZOLE; PROBIOTIC AGENT; RNA 16S; TUMOR NECROSIS FACTOR;

ANTIBIOTIC THERAPY; BACTERIAL OVERGROWTH; CONFUSION; FECAL MICROBIOTA TRANSPLANTATION; FERMENTED PRODUCT; FOOD ALLERGY; HUMAN; IMMUNOMODULATION; INTESTINE FLORA; LACTIC ACIDOSIS; LACTOBACILLUS; LOW BIRTH WEIGHT; MEMORY DISORDER; METAGENOMICS; MICROBIAL DIVERSITY; MICROBIOME; NECROTIZING ENTEROCOLITIS; PANCREATITIS; PERSONALIZED MEDICINE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SHORT TERM MEMORY; TRAVELLER DIARRHEA;

EID: 85066487330     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2019.00424     Document Type: Review

References (68)

1. Abubucker, S., Segata, N., Goll, J., Schubert, A. M., Izard, J., Cantarel, B. L., et al. (2012). Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comp. Biol. 8:e1002358. doi: 10.1371/journal.pcbi.1002358
2. Bae, J. M. (2018). Prophylactic efficacy of probiotics on travelers’ diarrhea: an adaptive meta-analysis of randomized controlled trials. Epidemiol. Health 40:e2018043. doi: 10.4178/epih.e2018043
3. Bajaj, J. S. (2019). Alcohol, liver disease and the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. doi: 10.1038/s41575-018-0099-1 [Epub ahead of print].
4. Besselink, M. G., Timmerman, H. M., Buskens, E., Nieuwenhuijs, V. B., Akkermans, L. M., Gooszen, H. G., et al. (2004). Probiotic prophylaxis in patients with predicted severe acute pancreatitis (PROPATRIA): design and rationale of a double-blind, placebo-controlled randomised multicenter trial [ISRCTN38327949]. BMC Surg. 4:12. doi: 10.1186/1471-2482-4-12
5. Besselink, M. G., van Santvoort, H. C., Renooij, W., de Smet, M. B., Boermeester, M. A., Fischer, K., et al. (2009). Intestinal barrier dysfunction in a randomized trial of a specific probiotic composition in acute pancreatitis. Ann. Surg. 250, 712–719. doi: 10.1097/SLA.0b013e3181bce5bd
6. Blander, J. M., Longman, R. S., Iliev, I. D., Sonnenberg, G. F., and Artis, D. (2017). Regulation of inflammation by microbiota interactions with the host. Nat. Immunol. 18:851. doi: 10.1038/ni.3780
7. Bogiatzi, C., Gloor, G., Allen-Vercoe, E., Reid, G., Wong, R. G., Urquhart, B. L., et al. (2018). Metabolic products of the intestinal microbiome and extremes of atherosclerosis. Atherosclerosis 273, 91–97. doi: 10.1016/j.atherosclerosis.2018.04.015
8. Bongaerts, G. P., and Severijnen, R. S. (2016). A reassessment of the PROPATRIA study and its implications for probiotic therapy. Nat. Biotechnol. 34, 55–63. doi: 10.1038/nbt.3436
9. Cox, M. A., Jackson, J., Stanton, M., Rojas-Triana, A., Bober, L., Laverty, M., et al. (2009). Short-chain fatty acids act as anti-inflammatory mediators by regulating prostaglandin E (2) and cytokines. World J. Gastroenterol. 15, 5549–5557. doi: 10.3748/wjg.15.5549
10. De Wolfe, T. J., Eggers, S., Barker, A. K., Kates, A. E., Dill-McFarland, K. A., Suen, G., et al. (2018). Oral probiotic combination of Lactobacillus and Bifidobacterium alters the gastrointestinal microbiota during antibiotic treatment for Clostridium difficile infection. PLoS One 13:e0204253. doi: 10.1371/journal.pone.0204253
11. Del Piano, M., Carmagnola, S., Anderloni, A., Andorno, S., Ballarè, M., Balzarini, M., et al. (2010). The use of probiotics in healthy volunteers with evacuation disorders and hard stools: a double-blind, randomized, placebo-controlled study. J. Clin. Gastroenterol. 44(Suppl. 1), S30–S34. doi: 10.1097/MCG.0b013e3181ee31c3
12. den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D. J., and Bakker, B. M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota and host energy metabolism. J. Lipid Res. 54, 2325–2340. doi: 10.1194/jlr.R036012
13. Desselberger, U. (2018). The mammalian intestinal microbiome: composition, interaction with the immune system, significance for vaccine efficacy, and potential for disease therapy. Pathogens 7:E57. doi: 10.3390/pathogens7030057
14. FAO/WHO (2002). Guidelines for the Evaluation of Probiotics in Food. Available At: https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf
15. Feehley, T., Plunkett, C. H., Bao, R., Choi Hong, S. M., Culleen, E., Belda-Ferre, P., et al. (2019). Healthy infants harbor intestinal bacteria that protect against food allergy. Nat. Med. doi: 10.1038/s41591-018-0324-z[Epub ahead of print].
16. Fiorucci, S., and Distrutti, E. (2015). Bile acid-activated receptors, intestinal microbiota, and the treatment of metabolic disorders. Trends Mol. Med. 21, 702–714. doi: 10.1016/j.molmed.2015.09.001
17. Fukui, H., Xu, X., and Miwa, H. (2018). Role of gut microbiota-gut hormone axis in the pathophysiology of functional gastrointestinal disorders. J. Neurogastroenterol. Motil. 24, 367–386. doi: 10.5056/jnm18071
18. Geva-Zatorsky, N., Sefik, E., Kua, L., Pasman, L., Tan, T. G., Ortiz-Lopez, A., et al. (2017). Mining the human gut microbiota for immunomodulatory organisms. Cell 168, 928–943. doi: 10.1016/j.cell.2017.01.022
19. Giamarellos-Bourboulis, E. J., Bengmark, S., Kanellakopoulou, K., and Kotzampassi, K. (2009). Pro- and synbiotics to control inflammation and infection in patients with multiple injuries. J. Trauma 67, 815–821. doi: 10.1097/TA.0b013e31819d979e
20. Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S., Reimer, R., Salminen, S., et al. (2017). Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the term and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14, 1–12. doi: 10.1038/nrgastro.2017.75
21. Global Market Insights (2016). Probiotics Market Size to Exceed USD 64 Billion by 2023: Global Market Insights Inc. Available at: https://www.prnewswire.com/news-releases/probiotics-marketsize-to-exceed-usd-64-billion-by-2023-global-market-insights-inc-578769201.html
22. Gottschick, C., Deng, Z., Vital, M., Masur, C., Abels, C., Pieper, D. H., et al. (2017). The urinary microbiota of men and women and its changes in women during bacterial vaginosis and antibiotic treatment. Microbiome 5:99. doi: 10.1186/s40168-017-0305-3
23. Hartstra, A. V., Bouter, K. E., Bäckhed, F., and Nieuwdorp, M. (2015). Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care 38, 159–165. doi: 10.2337/dc14-0769
24. Hentzer, M., and Givskov, M. (2003). Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Invest. 112, 1300–1307. doi: 10.1172/JCI20074
25. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D., Pot, B., et al. (2014). The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotics. Nat. Rev. Gastroenterol. Hepatol. 11, 506–514. doi: 10.1038/nrgastro.2014.66
26. Ho, L., Ono, K., Tsuji, M., Mazzola, P., Singh, R., and Pasinetti, G. M. (2018). Protective roles of intestinal microbiota derived short chain fatty acids in Alzheimer’s disease-type beta-amyloid neuropathological mechanisms. Expert Rev. Neurother. 18, 83–90. doi: 10.1080/14737175.2018.1400909
27. Hooks, K. B., Konsman, J. P., and O’Malley, M. A. (2018). Microbiota-gut-brain research: a critical analysis. Behav. Brain Sci. [Epub ahead of print]. doi: 10.1017/S0140525X18002133
28. Iemoli, E., Trabattoni, D., Parisotto, S., Borgonovo, L., Toscano, M., Rizzardini, G., et al. (2012). Probiotics reduce gut microbial translocation and improve adult atopic dermatitis. J. Clin. Gastroenterol. 46(Suppl.), S33–S40. doi: 10.1097/MCG.0b013e31826a8468
29. Karlsson, F. H., Fåk, F., Nookaew, I., Tremaroli, V., Fagerberg, B., Petranovic, D., et al. (2012). Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun. 3:1245. doi: 10.1038/ncomms2266
30. Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., and Gordon, J. I. (2011). Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336. doi: 10.1038/nature10213
31. Kim, Y. G., Sakamoto, K., Seo, S. U., Pickard, J. M., Gillilland, M. G. III, Pudlo, N. A., et al. (2017). Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens. Science 356, 315–319. doi: 10.1126/science.aag2029
32. Kleerebezem, M., Binda, S., Bron, P. A., Gross, G., Hill, C., van Hylckama Vlieg, J. E., et al. (2018). Understanding mode of action can drive the translational pipeline towards more reliable health benefits for probiotics. Curr. Opin. Biotechnol. 56, 55–60. doi: 10.1016/j.copbio.2018.09.007
33. Klemenak, M., Dolinšek, J., Langerholc, T., Di Gioia, D., and Mičetić-Turk, D. (2015). Administration of Bifidobacterium breve decreases the production of TNF-α in children with Celiac Disease. Dig. Dis. Sci. 60, 3386–3392. doi: 10.1007/s10620-015-3769-7
34. Kober, M., and Bowe, W. P. (2015). The effect of probiotics on immune regulation, acne, and photoaging. Int. J. Womens Dermatol. 1, 85–89. doi: 10.1016/j.ijwd.2015.02.001
35. Koppel, N., Rekdal, V. M., and Balskus, E. P. (2017). Chemical transformation of xenobiotics by the human gut microbiota. Science 356:eaag2770. doi: 10.1126/science.aag2770
36. Korpela, K., Salonen, A., Vepsäläinen, O., Suomalainen, M., Kolmeder, C., Varjosalo, M., et al. (2018). Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants. Microbiome 6:182. doi: 10.1186/s40168-018-0567-4
37. Ley, R. E., Turnbaugh, P. J., Klein, S., and Gordon, J. I. (2006). Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023. doi: 10.1038/4441022a
38. Magnúsdóttir, S., Ravcheev, D., de Crécy-Lagard, V., and Thiele, I. (2015). Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front. Genet. 6:148. doi: 10.3389/fgene.2015.00148
39. McCabe, L., Britton, R. A., and Parameswaran, N. (2015). Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr. Osteoporos. Rep. 13, 363–371. doi: 10.1007/s11914-015-0292-x
40. Morgan, X. C., Tickle, T. L., Sokol, H., Gevers, D., Devaney, K. L., and Ward, D. V. (2012). Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 13:R79. doi: 10.1186/gb-2012-13-9-r79
41. Nagpal, R., Wang, S., Ahmadi, S., Hayes, J., Gagliano, J., Subashchandrabose, S., et al. (2018). Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci Rep. 8:12649. doi: 10.1038/s41598-018-30114-4
42. Neuman, H., Debelius, J. W., Knight, R., and Koren, O. (2015). Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol. Rev. 39, 509–521. doi: 10.1093/femsre/fuu010
43. O’Mahony, S. M., Clarke, G., Borre, Y. E., Dinan, T. G., and Cryan, J. F. (2015). Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav. Brain Res. 277, 32–48. doi: 10.1016/j.bbr.2014.07.027
44. Patel, R. M., and Underwood, M. A. (2018). Probiotics and necrotizing enterocolitis. Semin. Pediatr. Surg. 27, 39–46. doi: 10.1053/j.sempedsurg.2017.11.008
45. Petrova, M. I., Macklaim, J., Wuyts, S., Verhoeven, T., Vanderleyden, J., Gloor, G. B., et al. (2018). Comparative genomic and phenotypic analysis of the vaginal probiotic Lactobacillus rhamnosus GR-1. Front. Microbiol. 9:1278. doi: 10.3389/fmicb.2018.01278
46. Quigley, E. M. M., Pot, B., and Sanders, M. E. (2018). ‘Brain fogginess’ and D-lactic acidosis: probiotics are not the cause. Clin. Transl. Gastroenterol. 9:187. doi: 10.1038/s41424-018-0057-9
47. Rao, S. S. C., Rehman, A., Yu, S., and Andino, N. M. (2018). Brain fogginess, gas and bloating: a link between SIBO, probiotics and metabolic acidosis. Clin. Transl. Gastroenterol. 9:162. doi: 10.1038/s41424-018-0030-7
48. Reid, G., Gibson, G., Sanders, M. E., Guarner, F., and Versalovic, J. (2008). Probiotic prophylaxis in predicted severe acute pancreatitis. Lancet 372, 112–113. doi: 10.1016/S0140-6736(08)61024-7
49. Resta-Lenert, S., and Barrett, K. E. (2006). Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130, 731–746. doi: 10.1053/j.gastro.2005.12.015
50. Sanders, M. E., Hamilton, J., Reid, G., and Gibson, G. (2007). A nonviable preparation of Lactobacillus acidophilus is not a probiotic. Clin. Infect. Dis. 44:886.
51. Sanders, M. E., Merenstein, D. J., Ouwehand, A. C., Reid, G., Salminen, S., Cabana, M. D., et al. (2016). Probiotic use in at-risk populations. J. Am. Pharm. Assoc. 56, 680–686. doi: 10.1016/j.japh.2016.07.001
52. Savidge, T. C. (2016). Epigenetic regulation of enteric neurotransmission by gut bacteria. Front. Cell. Neurosci. 9:503. doi: 10.3389/fncel.2015.00503
53. Schirmer, M., Franzosa, E. A., Lloyd-Price, J., McIver, L. J., Schwager, R., and Poon, T. W. (2018). Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat. Microbiol. 3, 337–346. doi: 10.1038/s41564-017-0089-z
54. Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly-Y, M., et al. (2013). The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569–573. doi: 10.1126/science.1241165
55. Sonnenburg, J. L., and Bäckhed, F. (2016). Diet–microbiota interactions as moderators of human metabolism. Nature 535, 56–64. doi: 10.1038/nature18846
56. Suez, J., Zmora, N., Zilberman-Schapira, G., Mor, U., Dori-Bachash, M., Bashiardes, S., et al. (2018). Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174, 1406–1423.e16. doi: 10.1016/j.cell.2018.08.047
57. Tang, W. H., Wang, Z., Levison, B. S., Koeth, R. A., Britt, E. B., Fu, X., et al. (2013). Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N. Engl. J. Med. 368, 1575–1584. doi: 10.1056/NEJMoa1109400
58. Tang, W. W., and Hazen, S. L. (2014). The contributory role of gut microbiota in cardiovascular disease. J. Clin. Invest. 124, 4204–4211. doi: 10.1172/JCI72331
59. Thaiss, C. A., Zmora, N., Levy, M., and Elinav, E. (2016). The microbiome and innate immunity. Nature 535, 65–74. doi: 10.1038/nature18847
60. Valles-Colomer, M., Falony, G., Darzi, Y., Tigchelaar, E. F., Wang, J., Tito, R. Y., et al. (2019). The neuroactive potential of the human gut microbiota in quality of life and depression. Nat. Microbiol. doi: 10.1038/s41564-018-0337-x [Epub ahead of print].
61. Vitetta, L., Coulson, S., Thomsen, M., Nguyen, T., and Hall, S. (2017). Probiotics, D-Lactic acidosis, oxidative stress and strain specificity. Gut Microbes 8, 311–322. doi: 10.1080/19490976.2017.1279379
62. Wandro, S., Osborne, S., Enriquez, C., Bixby, C., Arrieta, A., and Whiteson, K. (2018). The microbiome and metabolome of preterm infant stool are personalized and not driven by health outcomes, including necrotizing enterocolitis and late-onset sepsis. mSphere 3, e104-18. doi: 10.1128/mSphere.00104-18
63. Weiss, G. A., and Hennet, T. (2017). Mechanisms and consequences of intestinal dysbiosis. Cell. Mol. Life Sci. 74, 2959–2977. doi: 10.1007/s00018-017-2509-x
64. Yan, J., Herzog, J. W., Tsang, K., Brennan, C. A., Bower, M. A., and Garrett, W. S. (2016). Gut microbiota induce IGF-1 and promote bone formation and growth. Proc. Nat. Acad. Sci. U.S.A. 113, E7554–E7563. doi: 10.1073/pnas.1607235113
65. Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., and Ma, L. (2015). Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161, 264–276. doi: 10.1016/j.cell.2015.02.047
66. Zeng, M. Y., Cisalpino, D., Varadarajan, S., Hellman, J., Warren, H. S., and Cascalho, M. (2016). Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44, 647–658. doi: 10.1016/j.immuni.2016.02.006
67. Zhang, Y., Brady, A., Jones, C., Song, Y., Darton, T. C., Jones, C., et al. (2018). Compositional and functional differences in the human gut microbiome correlate with clinical outcome following infection with wild-type Salmonella enterica serovar Typhi. mBio 9:e686-18. doi: 10.1128/mBio.00686-18
68. Zmora, N., Zilberman-Schapira, G., Suez, J., Mor, U., Dori-Bachash, M., Bashiardes, S., et al. (2018). Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174, 1388–1405.e22. doi: 10.1016/j.cell.2018.08.041