Dealing with the remaining controversies of probiotic safety

Beneficial Microbes

Volumn 10, Issue 6, 2019, Pages 605-616

  Van Den Nieuwboer, M ^a   Claassen, E ^a  

^a ATHENA INSTITUTE   (Netherlands)

Author keywords

Acute pancreatitis; Probiotics; PROPATRIA; Safety; Safety reporting

Indexed keywords

PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; SYNBIOTIC AGENT; ANTIINFECTIVE AGENT;

ACUTE PANCREATITIS; ARTICLE; BACTERIAL OVERGROWTH; BIFIDOBACTERIUM; CLOSTRIDIUM DIFFICILE INFECTION; CRITICALLY ILL PATIENT; DRUG MECHANISM; DRUG SAFETY; HEALTH HAZARD; HUMAN; INFECTION; INFLAMMATION; INTENSIVE CARE UNIT; INTESTINE FLORA; INTESTINE ISCHEMIA; INTESTINE MOTILITY; LACTOBACILLUS; MORTALITY; NECROTIZING ENTEROCOLITIS; NONHUMAN; PERMEABILITY BARRIER; RISK BENEFIT ANALYSIS; RISK FACTOR; STANDARDIZATION; CLINICAL DECISION MAKING; CLINICAL TRIAL (TOPIC); CRITICAL ILLNESS; PANCREATITIS;

ANTI-BACTERIAL AGENTS; CLINICAL DECISION-MAKING; CLINICAL TRIALS AS TOPIC; CRITICAL ILLNESS; HUMANS; PANCREATITIS; PROBIOTICS; SYNBIOTICS;

EID: 85069466252     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2018.0159     Document Type: Article

References (66)

1. AlFaleh, K. and Anabrees, J., Bassler, D. and Al-Kharfi, T., 2014. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Evidence-Based Child Health: A Cochrane Review Journal 9: 584-671.
2. Bafeta, A., Koh, M., Riveros, C. and Ravaud, P., 2018. Harms reporting in randomized controlled trials of interventions aimed at modifying microbiota: a systematic review. Annals of Internal Medicine 169: 240-247.
3. Banks, P.A. and Freeman, M.L., 2006. Practice guidelines in acute pancreatitis. American Journal of Gastroenterology 101: 2379-2400.
4. Barraud, D., Blard, C., Hein, F., Marçon, O., Cravoisy, A., Nace, L., Alla, F., Bollaert, P.E. and Gibot, S., 2010. Probiotics in the critically ill patient: a double blind, randomized, placebo-controlled trial. Intensive Care Medicine 36: 1540-1547.
5. Besselink, M.G., Timmerman, H.M., Buskens, E., Nieuwenhuijs, V.B., Akkermans, L.M. and Gooszen, H.G., 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 Surgery 4: 12.
6. Besselink, M.G., Van Santvoort, H.C., Boermeester, M.A., Nieuwenhuijs, V.B., Van Goor, H., Dejong, C.H.C. and Gooszen, H.G., 2009. Timing and impact of infections in acute pancreatitis. British Journal of Surgery: Incorporating European Journal of Surgery and Swiss Surgery 96: 267-273.
7. Besselink, M.G., Van Santvoort, H.C., Buskens, E., Boermeester, M.A., Van Goor, H., Timmerman, H.M. and Rosman, C., 2008a. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. The Lancet 371: 651-659.
8. Besselink, M.G., Van Santvoort, H.C., Renooij, W., De Smet, M.B., Boermeester, M.A., Fischer, K. and Van Ramshorst, B., 2008b. Intestinal barrier dysfunction in a randomised placebo-controlled trial of probiotic prophylaxis in acute pancreatitis. European Journal of Gastroenterology and Hepatology 15: A1-A76.
9. Blum, H.E., 2017. The human microbiome. Advances in Medical Sciences 62: 414-420.
10. Bongaerts, G.P. and Severijnen, R.S., 2016. A reassessment of the PROPATRIA study and its implications for probiotic therapy. Nature Biotechnology 34: 55.
11. Boyle, R.J., Robins-Browne, R.M. and Tang, M.L., 2006. Probiotic use in clinical practice: what are the risks? American Journal of Clinical Nutrition 83: 1256-1264.
12. Cuello-Garcia, C.A., Brożek, J.L., Fiocchi, A., Pawankar, R., Yepes- Nuñez, J.J., Terracciano, L. and Schünemann, H.J., 2015. Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. Journal of Allergy and Clinical Immunology 136: 952-961.
13. Demirel, G., Erdeve, O., Celik, I.H. and Dilmen, U., 2013. Saccharomyces boulardii for prevention of necrotizing enterocolitis in preterm infants: a randomized, controlled study. Acta Paediatrica 102: e560-e565.
14. Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X. and Zhang, T., 2017. The 'golden age' of probiotics: a systematic review and meta-analysis of randomized and observational studies in preterm infants. Neonatology 112: 9-23.
15. Didari, T., Solki, S., Mozaffari, S., Nikfar, S. and Abdollahi, M., 2014. A systematic review of the safety of probiotics. Expert Opinion on Drug Safety 13: 227-239.
16. Dilli, D., Aydin, B., Fettah, N.D., Özyazici, E., Beken, S., Zenciroǧlu, A. and Turan, Ö., 2015. The propre-save study: effects of probiotics and prebiotics alone or combined on necrotizing enterocolitis in very low birth weight infants. Journal of Pediatrics 166: 545-551.
17. Doron, S. and Snydman, D.R., 2015. Risk and safety of probiotics. Clinical Infectious Diseases 60: S129-S134.
18. Flach, J., Van der Waal, M.B., Van den Nieuwboer, M., Claassen, E. and Larsen, O.F., 2017. The underexposed role of food matrices in probiotic products: reviewing the relationship between carrier matrices and product parameters. Critical Reviews in Food Science and Nutrition 58: 2570-2584.
19. Floch, M.H., Walker, W.A., Sanders, M.E., Nieuwdorp, M., Kim, A.S., Brenner, D.A. and Dieleman, L.A., 2015. Recommendations for probiotic use - 2015 update: proceedings and consensus opinion. Journal of Clinical Gastroenterology 49: S69-S73.
20. Gallagher, J., 2018. Probiotics labelled 'quite useless'. BBC. Available at: https://www.bbc.com/news/health-45434753
21. Gil-Campos, M., López, M.Á., Rodriguez-Benítez, M.V., Romero, J., Roncero, I., Linares, M.D. and Navas, V., 2012. Lactobacillus fermentum CECT 5716 is safe and well tolerated in infants of 1-6 months of age: a randomized controlled trial. Pharmacological Research 65: 231-238.
22. Goldenberg, J.Z., Yap, C., Lytvyn, L., Lo, C.K.F., Beardsley, J., Mertz, D. and Johnston, B.C., 2017. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Library: CD006095.
23. Gooszen, H.G., 2010. The PROPATRIA trial: best practices at the time were followed. The Lancet 375: 1249-1250.
24. Gou, S., Yang, Z., Liu, T., Wu, H. and Wang, C., 2014. Use of probiotics in the treatment of severe acute pancreatitis: a systematic review and meta-analysis of randomized controlled trials. Critical Care 18: R57.
25. Hao, Q., Dong, B.R. and Wu, T., 2015. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Systematic Reviews 2: CD006895.
26. Hempel, S., Newberry, S., Ruelaz, A., Wang, Z., Miles, J.N., Suttorp, M.J. and Smith, A., 2011. Safety of probiotics used to reduce risk and prevent or treat disease. Evidence Report/Technology Assessment 1-645.
27. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B. and Calder, P.C., 2014. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology and Hepatology 11: 506.
28. Hojsak, I., Fabiano, V., Pop, T.L., Goulet, O., Zuccotti, G.V., Çokuǧraş, F.C. and Kolaček, S., 2018. Guidance on the use of probiotics in clinical practice in children with selected clinical conditions and in specific vulnerable groups. Acta Paediatrica 107: 927-937.
29. Horst, N.L., Marques, R.G., Diestel, C.F., Matzke, B.D., Caetano, C.E.R., Simões, F.C. and Braga, J.U., 2009. Effects of probiotic supplementation on markers of acute pancreatitis in rats. Current Therapeutic Research 70: 136-148.
30. Liu, Z., Qin, H., Yang, Z., Xia, Y., Liu, W., Yang, J. and Zheng, Q., 2011. Randomised clinical trial: the effects of perioperative probiotic treatment on barrier function and post-operative infectious complications in colorectal cancer surgery - a double-blind study. Alimentary Pharmacology and Therapeutics 33: 50-63.
31. Maldonado, J., Cañabate, F., Sempere, L., Vela, F., Sánchez, A.R., Narbona, E. and Lara-Villoslada, F., 2012. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. Journal of Pediatric Gastroenterology and Nutrition 54: 55-61.
32. Manzanares, W., Lemieux, M., Langlois, P.L. and Wischmeyer, P.E., 2016. Probiotic and synbiotic therapy in critical illness: a systematic review and meta-analysis. Critical Care 20: 262.
33. Manzoni, P., Gallo, E. and Farina, D., 2009. Probiotics for the neonate. Journal of Maternal-Fetal and Neonatal Medicine 22: 27-30.
34. Markowiak, P. and Śliżewska, K., 2017. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9: 1021.
35. Morrow, L.E. and Wischmeyer, P.E., 2017. Blurred lines: dysbiosis and probiotics in the ICU. Chest 151: 492-499.
36. Morrow, L.E., Gogineni, V. and Malesker, M.A., 2012. Synbiotics and probiotics in the critically ill after the PROPATRIA trial. Current Opinion in Clinical Nutrition and Metabolic Care 15: 147-150.
37. Muftuoglu, M.A.T., Isikgor, S., Tosun, S. and Saglam, A., 2006. Effects of probiotics on the severity of experimental acute pancreatitis. European Journal of Clinical Nutrition 60: 464.
38. Oláh, A., Belagyi, T., Issekutz, A., Gamal, M.E. and Bengmark, S., 2002. Randomized clinical trial of specific lactobacillus and fibre supplement to early enteral nutrition in patients with acute pancreatitis. British Journal of Surgery 89: 1103-1107.
39. Oláh, A., Belágyi, T., Pótó, L., Romics, L. and Bengmark, S., 2007. Synbiotic control of inflammation and infection in severe acute pancreatitis: a prospective, randomized, double blind study. Hepato- Gastroenterology 54: 590-594.
40. Parker, E.A., Roy, T., D'Adamo, C.R. and Wieland, L.S., 2017. Probiotics and gastrointestinal conditions: an overview of evidence from the Cochrane Collaboration. Nutrition 45: 125-134.
41. Poropat, G., Giljaca, V., Hauser, G. and Štimac, D., 2015. Enteral nutrition formulations for acute pancreatitis. Cochrane Database of Systematic Reviews 3: CD010605.
42. Rayes, N., Hansen, S., Seehofer, D., Müller, A.R., Serke, S., Bengmark, S. and Neuhaus, P., 2002a. Early enteral supply of fiber and lactobacilli versus conventional nutrition: a controlled trial in patients with major abdominal surgery. Nutrition 18: 609-615.
43. Rayes, N., Seehofer, D., Hansen, S., Boucsein, K., Müller, A.R., Serke, S. and Neuhaus, P., 2002b. Early enteral supply of Lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 74: 123-128.
44. Ridwan, B.U., Besselink, M.G.H., Koning, C., Timmerman, H.M., Verhoef, J., Gooszen, H.G. and Akkermans, L.M.A., 2005. Prevention of secondary pancreatic infections with probiotics; in vitro studies. European Journal of Gastroenterology and Hepatology 17: A42-A43.
45. Ridwan, B.U., Koning, C.J.M., Besselink, M.G.H., Timmerman, H.M., Brouwer, E.C., Verhoef, J. and Akkermans, L.M.A., 2008. Antimicrobial activity of a multispecies probiotic (Ecologic 641) against pathogens isolated from infected pancreatic necrosis. Letters in Applied Microbiology 46: 61-67.
46. Romeo, M.G., Romeo, D.M., Trovato, L., Oliveri, S., Palermo, F., Cota, F. and Betta, P., 2011. Role of probiotics in the prevention of the enteric colonization by Candida in preterm newborns: incidence of late-onset sepsis and neurological outcome. Journal of Perinatology 31: 63.
47. Samanta, M., Sarkar, M., Ghosh, P. and Chatterjee, S., 2009. Prophylactic probiotics for prevention of necrotizing enterocolitis in very low birth weight newborns. Journal of Tropical Paediatrics 55: 128-131.
48. Sharma, B., Srivastava, S., Singh, N., Sachdev, V., Kapur, S. and Saraya, A., 2011. Role of probiotics on gut permeability and endotoxemia in patients with acute pancreatitis: a double-blind randomized controlled trial. Journal of Clinical Gastroenterology 45: 442-448.
49. Suez, J., Zmora, N., Zilberman-Schapira, G., Mor, U., Dori-Bachash, M., Bashiardes, S. and Horn, M., 2018. Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174: 1406-1423.
50. The Guardian, 2018. Probiotics 'not as beneficial for gut health as previously thought. Available at: https://tinyurl.com/y7bwve57.
51. Tian, X., Pi, Y.P., Liu, X.L., Chen, H. and Chen, W.Q., 2018. Supplemented use of pre-, pro-and synbiotics in severe acute pancreatitis: an updated systematic review and meta-analysis of 13 randomized controlled trials. Frontiers in Pharmacology 9: 690.
52. Underwood, M.A., 2019. Probiotics and the prevention of necrotizing enterocolitis. Journal of Pediatric Surgery 54: 405-412.
53. Usami, M., Miyoshi, M., Kanbara, Y., Aoyama, M., Sakaki, H., Shuno, K. and Asahara, T., 2011. Effects of perioperative synbiotic treatment on infectious complications, intestinal integrity, and fecal flora and organic acids in hepatic surgery with or without cirrhosis. Journal of Parenteral and Enteral Nutrition 35: 317-328.
54. Van Baal, M.C., 2014. Acute pancreatitis: persisting issues from the PROPATRIA and PANTER studies. PhD-thesis, Radboud University, Nijmegen, the Netherlands.
55. Van Baal, M.C., Van Rens, M.J., Geven, C.B., Van de Pol, F.M., Van den Brink, I.W., Hannink, G. and Gooszen, H.G., 2014. Association between probiotics and enteral nutrition in an experimental acute pancreatitis model in rats. Pancreatology 14: 470-477.
56. Van de Burgwal, L.H.M, Van der Waal, M. and Claassen, H.J.H.M., 2018. Leveraging academic knowledge in the innovation ecosystem. Stichting Maatschappij en Onderneming (SMO). Available at: http://hdl.handle.net/1765/104386.
57. Van den Nieuwboer, M., Browne, P.D. and Claassen, E., 2017. Chapter 17 Safety of probiotics in infants and children. In: Browne, P.D., Claassen, E. and Cabana, M.D. (eds.) Microbiota in health and disease: from pregnancy to childhood. Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 17-23.
58. Van den Nieuwboer, M., Brummer, R.J., Guarner, F., Morelli, L., Cabana, M. and Claassen, E., 2014b. The administration of probiotics and synbiotics in immune compromised adults: is it safe? Beneficial Microbes 6: 3-17.
59. Van den Nieuwboer, M., Brummer, R.J., Guarner, F., Morelli, L., Cabana, M. and Claassen, E., 2015. Safety of probiotics and synbiotics in children under 18 years of age. Beneficial Microbes 6: 615-630.
60. Van den Nieuwboer, M., Claassen, E., Morelli, L., Guarner, F. and Brummer, R.J., 2014a. Probiotic and synbiotic safety in infants under two years of age. Beneficial Microbes 5: 45-60.
61. Van den Nieuwboer, M., Van de Burgwal, L.H.M. and Claassen, E., 2016. A quantitative key-opinion-leader analysis of innovation barriers in probiotic research and development: valorisation and improving the tech transfer cycle. Pharma Nutrition 4: 9-18.
62. Van Minnen, L.P., Timmerman, H.M., Lutgendorff, F., Verheem, A., Harmsen, W., Konstantinov, S. R. and Akkermans, L.M., 2007. Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis. Surgery 141: 470-480.
63. Vandenplas, Y. and Huysentruyt, K., 2017. Probiotic interventions to optimise the infant and child microbiota. In: Browne, P.D., Claassen, E. and Cabana, M.D. (eds.) Microbiota in health and disease: from pregnancy to childhood. Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 62.
64. Zeilstra, D., Younes, J.A., Brummer, R.J. and Kleerebezem, M., 2018. Perspective: fundamental limitations of the randomized controlled trial method in nutritional research: the example of probiotics. Advances in Nutrition 9: 561-571.
65. Zhang, J.W., Du, P., Yang, B.R., Gao, J., Fang, W.J. and Ying, C.M., 2012. Preoperative probiotics decrease postoperative infectious complications of colorectal cancer. American Journal of the Medical Sciences 343: 199-205.
66. Zmora, N., Zilberman-Schapira, G., Suez, J., Mor, U., Dori-Bachash, M., Bashiardes, S. and Federici, S., 2018. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174: 1388-1405.