Are probiotic really safe for humans?

Polish Journal of Microbiology

Volumn 67, Issue 3, 2018, Pages 251-258

  Zawistowska Rojek, Anna ^a   Tyski, Stefan ^a,b  

^a NATIONAL MEDICINES INSTITUTE   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Bacteremia; Gene transfer; Probiotic bacteria; Probiotic side effect; Safety of probiotics

Indexed keywords

PROBIOTIC AGENT;

BACTEREMIA; BACTERIAL STRAIN; BIOSAFETY; DEVICE SAFETY; DRUG SAFETY; FOOD SAFETY; HORIZONTAL GENE TRANSFER; HUMAN; IMMUNOSTIMULATION; INTESTINE FLORA; LACTOBACILLUS; METABOLISM; NONHUMAN; REVIEW; RISK ASSESSMENT; BIFIDOBACTERIUM; IMMUNOCOMPROMISED PATIENT; PRODUCT SAFETY;

BACTEREMIA; BIFIDOBACTERIUM; CONSUMER PRODUCT SAFETY; GENE TRANSFER, HORIZONTAL; HUMANS; IMMUNOCOMPROMISED HOST; LACTOBACILLUS; PROBIOTICS;

EID: 85052995998     PISSN: 17331331     EISSN: None     Source Type: Journal    
DOI: 10.21307/pjm-2018-044     Document Type: Review

References (96)

1. Abe F, Muto M, Yaeshima T, Iwatsuki K, Aihara H, Ohashi Y, Fujisawa T. 2010. Safety evaluation of probiotic bifidobacteria by analysis of mucin degradation activity and translocation ability. Anaerobe. 16:131–136.
2. Agostoni C, Salvini F. 2009. Probiotics in Infant Dietetics. In: Michail S, Sherman PM, editors. Probiotics in Pediatric Medicine. New York (USA): Humana Press.
3. Ambesh P, Stroud S, Franzova E, Gotesman J, Sharma K, Wolf L, Kamholz S. 2017. Recurrent Lactobacillus bacteremia in a patient with leukemia. J Investig Med High Impact Case Rep. 5:1–3.
4. Ammor MS, Florez AB, Mayo B. 2007. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 24:559–570.
5. Ashraf A, Shah NP. 2011. Antibiotic resistance of probiotic organisms and safety of probiotic dairy products. Int Food Res J. 18:837–853.
6. Bayer AS, Chow AW, Betts D, Guze LB. 1978. Lactobacillemia: report of 9 cases: important clinical and therapeutic considerations. Am J Med. 64:808–813.
7. Belletti N, Gatti M, Bottari B, Neviani E, Tabanelli G, Gardinni F. 2009. Antibiotic resistance of lactobacilli isolated from two Italian hard cheeses. J Food Prot. 72:2162–2169.
8. Berg RD. 1985. Bacterial translocation from the intesties. Exp Anim. 34:1–16.
9. Berg RD. 1992. Translocation and the indigenous gut flora. In: Fuller R. Probiotics: The Scientific Basis. London (UK): Chapman & Hall. p. 55–85.
10. Bongaerts G, Bakkeren J, Severijnen R, Sperl W, Willems H, Naber T, Wevers R, van Meurs A, Tolboom J. 2000. Lactobacilli and acidosis in children with short small bowel. J Pediatr Gastroenterol Nutr. 30:288–293.
11. Borriello SP, Hammes WP, Holzapfel W, Marteau P, Schhrezen-meir J, Vaara M, Valtonen V. 2003. Safety of probiotics that contain lactobacilli and bifidobacteria. Clin Infect Dis. 36:775–780.
12. Boyle RJ, Robins-Browne RM, Tang ML. 2006. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr. 83:1256–1264.
13. Brook I. 1996. Isolation of non-sporing anaerobic rods from infections in children. J Med Microbiol. 45:21–26.
14. Brughton RA, Gruber WC, Haffar AA, Baker CJ. 1983. Neonatal meningitis due to Lactobacillus. Pediatr Infect Dis J. 2:382–384.
15. Brumfitt W, Ludlam H, Hamilton-Miller JMT, Gooding A. 1981. Lactobacilli do not cause frequency and dysuria a syndrome. Lancet. 2:393–395
16. Burkhardt O, Köhnlein T, Pletz M, Welte T. 2005. Saccharomyces boulardii induced sepsis: successful therapy with voriconazole after treatment failure with fluconazole. Scand J Inf Dis. 37:69–72.
17. Charteris WP, Kelly PM, Morelli L, Collins JK. 1998. Antibiotic susceptibility of potentially probiotic Lactobacillus species. J Food Prot. 61:1636–1643.
18. Coeuret V, Gueguen M, Vernoux JP. 2004. Numbers and strains of lactobacilli in some probiotic products. Int J Food Microbiol. 97:147–156.
19. De Groote MA, Frank DN, Dowell E, Glode MP, Pace NR. 2005. Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Ped Infect Dis J. 24:278–280.
20. Dessart SR, Steenson LR. 1991. High frequency intergeneric and intrageneric conjugal transfer of drug resistance plasmids in Leuconostoc mesenteroides ssp cremoris. J Dairy Sci. 74:2912–2919.
21. Dickgieber U, Weiss N, Fritsche D. 1984. Lactobacillus gasseri as the cause of septic urinary infection. Infection. 12:14–16.
22. Doron S, Snydman DR. 2015. Risk and safety of probiotics. Clin Infect Dis. 60(Suppl 2):129–134.
23. European Food Safety Authority. 2012. Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10(2740):1–10.
24. Fukao M, Yajima N. 2012. Assessment of antibiotic resistance in probiotic lactobacilli. In: Pana M, editor. Antibiotic resistant bacteria – A continuous challenge in the new millennium. London (UK): IntechOpen [Internet]. doi: 10.5772/30903; [cited 2017 December 20]. Available from: http://www.intechopen.com/books/antibioticresistant-bacteria-a-continuous-challenge-in-the-new-millennium/ assessment-of-antibiotic-resistance-in-probiotic-strains
25. Gevers D, Danielsen M, Huys G, Swings J. 2003a. Molecular characterization of tet(M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol. 69:1270–1275.
26. Gevers D, Huys G, Swings J. 2003b. In vitro conjugal transfer of tetracycline resistance from Lactobacillus isolates to other Gram-positive bacteria. FEMS Microbiol Lett. 225:125–130.
27. Global Market Insights [Internet]. 2017. Los Ageles (USA): Globe-Newswire; [cited 2018 March 14]. Available from: globenewswire. com/news-release/2017/10/10/1143574/0/en/Probiotics-Market-to-exceed-65bn-by-2024-Global-Market-Insights-Inc.html
28. Gueimonde M, Ouwehand AC, Salminen S. 2004. Safety of probiotics. Scand J Nutr. 48:42–48.
29. Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, Zhang H, Zhang W. 2017. Characterization of antibiotic resistance genes from lactobacillus isolated from traditional dairy products. J Food Sci. 82:724–730.
30. Harty DWS, Oakey HJ, Patrikakis M, Hume EBH, Knox KW. 1994. Pathogenic potential of lactobacilli. Int J Food Microbiol. 24:179–189.
31. Harty DWS, Patrikakis M, Knox KW. 1993. Identification of Lactobacillus strains from patients with infective endocarditis and comparison of their surface-associated properties with those of other strains of the same species. Microb Ecol Health Dis. 6:191–201.
32. Hempel S, Newberry S, Ruelaz A, Wang Z, Miles JN, Suttorp MJ, Johansen B, Shanman R, Slusser W, Fu N, et al. 2011. Safety of probiotics used to reduce risk and prevent or treat disease. Evid Rep Technol Assess. 200:1–645.
33. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S. 2014. Expert consensus document”The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic”. Nat Rev Gastroenterol Hepatol. 11:506–514.
34. Hoa NT, Baccigalupi L, Huxham A, Smertenko A, Van PH, Ammendola S, Ricca E, Cutting AS. 2000. Characterization of Bacillus species used for oral bacteriotherapy and bacteriopro-phylaxis of gastrointestinal disorders. Appl Environ Microbiol. 66: 5241–5247.
35. Horwitch CA, Furseth HA, Larson AM, Jones TL, Olliffe JF, Spach DH. 1995. Lactobacillemia in three patients with AIDS. Clin Infect Dis. 21:1460–1462.
36. Hove H, Mortensen PB. 1995. Influence of intestinal inflammation (IBD) and small and large-bowel length on fecal short-chain fatty-acids and lactate. Dig Dis Sci. 40:1372–1380.
37. Ishibashi N, Yamazaki S. 2001. Probiotics and safety. Am J Clin Nutr. 73(Suppl):465S–470S.
38. Johnson BR, Klaenhammer TR. 2014. Impact of genomics on the field of probiotic research: historical perspectives to modern paradigms. Antoine van Leeuwenhoek. 106:141–156.
39. Kalima P, Masterton RG, Roddie PH, Thomas AE. 1996. Lactobacillus rhamnosus infection in a child following bone marrow transplant. J Infect. 32:165–167.
40. Kochan P, Chmielarczyk A, Szymaniak L, Brykczynski M, Galant K, Zych A, Pakosz K, Giedrys-Kalemba S, Lenouvel E, Heczko PB. 2011. Lactobacillus rhamnosus administration causes sepsis in a cardiosurgical patient – is the time right to revise probiotic safety guidelines? Clin Microbiol Infect. 17:1589–1592.
41. Kunz AN, Noel JM, Fairchok MP. 2004. Two cases of Lactobacillus bacteremia during probiotc treatment of short gut syndrome. J Ped Gastroent Nutr. 38:457–458.
42. Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. 2005. Lactobacillus sepsis associated with probiotic therapy. Pediatrics. 115:178–181.
43. Ledoux D, Labombardi VJ, Karter D. 2006. Lactobacillus acidophilus bacteremia after use of a probiotic in a patient with AIDS and Hodgkin`s disease. Int J STD AIDS. 17:280–282.
44. Lee TT, Morisset M, Astier C, Moneret-Vautrin DA, Cordebar V, Beaudouin E, Codreanu F, Bihain BE, Kanny G. 2007. Contamination of probiotic preparations with milk allergens can cause ana-phylaxis in children with cow’s milk allergy. J Allergy Clin Immunol. 119:746–747.
45. Lilly DM, Stillwell RH. 1965. Growth promoting factors produced by probiotics. Science. 147:747–748.
46. Liong MT. 2008. Safety of probiotics: translocation and infection. Nutr Rev. 66:192–202.
47. Liu Ch, Zhang Z, Dong K, Yuan J, Guo X. 2009. Antibiotic resistance of probiotic strains of lactic acid bacteria isolated from marketed foods and drugs. Biomed Env Sci. 22:401–412.
48. Łukasik J, Salminen S, Szajewska H. 2018. Rapid review shows that probiotics and fermented infant formulas do not cause D-lactic acidosis in healthy children. Acta Paediatr. 107:1322–1326.
49. Masco L, Huys G, De Brandt E, Temmerman R, Swings J. 2005. Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol. 102:221–230.
50. Mathur S, Singh R. 2005. Antibiotic resistance in food lactic acid bacteria – a review. Int J Food Microbiol. 105:281–295.
51. McFarland LV. 2015. From yaks to yogurt: the history, development, and current use of probiotics. Clin Infect Dis. 60(S2):S85–S90.
52. Metchnikoff E. 1908. The prolongation of life. Optimistic studies. New York (USA): Putnam’s Sons. p. 161–183.
53. Milazzo I, Speciale A, Musumeci R, Fazio D, Blandino G. 2006. Identification and antibiotic susceptibility of bacterial isolates from probiotic products available in Italy. New Microbiol. 29: 281–291.
54. Moneret-Vautrin DA, Morisset M, Cordebar V, Codreanu F, Kanny G. 2006. Probiotics may be unsafe in infants allergic to cow’s milk. Allergy. 61:507–508.
55. Morelli L, Sarra PG, Bottazzi V. 1988. In vivo transfer of pAM beta 1 from Lactobacillus reuteri to Enterococcus faecalis. J Appl Bacteriol. 65:371–375.
56. Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F. 2005. Antimicrobial susceptibility of Bifidobacteria. J Antimicrob Chemother. 55:38–44.
57. Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Millar BC, Xu J. 2011. Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol. 62:1081–1089.
58. Ooi LG, Liong MT. 2010. Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int J Mol Sci. 11:2499–2522.
59. Ouwehand AC, Saxelin M, Salminen S. 2004. Phenotypic differences between commercial Lactobacillus rhamnosus GG and L.rhamnosus strains recovered from blood. Clin Infect Dis. 39: 1858–1860.
60. Patel R, Cockerill FR, Porayko MK, Osmon DR, Ilstrump DM, Keating MR. 1994. Lactobacillemia in liver transplant patients. Clin Infect. 18:207–212.
61. Report FAO/WHO. 2001. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria [Internet]. p. 1–29; [cited 2017 November 15]. Available from: http://www.fao.org/tempref/docrep/fao/meeting/009/y6398e.pdf
62. Report FAO/WHO. 2002. Report of a Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food [Internet]. p. 36–48; [cited 2017 November 15]. Available from: http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf
63. Ruseler-van Embden JGH, van Lieshout LMC, Gosselink MJ, Marteau P. 1995. Inability of Lactobacillus casei strain GG, L. acidophilus, and Bifidobacterium bifidum to degrade intestinal mucus glycoproteins: clearing the way for mucosa-protective therapy. Scand J Gastroenterol. 30:675–680.
64. Saarela M, Mogensen G, Fonden R, Matto J, Mattila-Sandholm T. 2000. Probiotic bacteria: safety, functional and technological properties. J Biotechnol. 84:197–215.
65. Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V, Järvinen A. 2004. Lactobacillus bacteremia, clinical signifiance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis. 38:62–69.
66. Salminen MK, Tynkkynen S, Rautelin H, Saxelin M, Vaara M, Ruutu P, Sarna S, Valtonen V, Järvinen A. 2002. Lactobacillus bacteremia during a rapid increase in probiotic use f Lactobacillus rhamnosus GG in Finland. Clin Infect Dis. 35:1155–1160.
67. Salyers AA, Gupta A, Wang Y. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 12:412–416.
68. Sanders ME, Akkermans LMA, Haller D, Hammerman C, Heimbach J, Hormannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, et al. 2010. Safety assessment of probiotic for human use. Gut Microbes. 1:164–185.
69. Sanders ME, Klaenhammer TR, Ouwehand AC, Pot B, Johanses E, Heimbach JT, Marco ML, Tenilä J, Ross RP, Franz C, et al. 2014. Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics. Ann N.Y. Acad Sci. 1309:1–18.
70. Schjørring S, Krogfelt KA. 2011. Assessment of bacterial antibiotic resistance transfer in the gut. Int J Microbiol [Internet]:1–10; [cited 2017 December 17]. Available from: http://dx.doi.org/10.1155/2011/312956
71. Schlegel L, Lemerle S, Geslin P. 1998. Lactobacillus species as opportunistic pathogens in immunocompromised patients. Eur J Clin Microbiol Infect. 17:887–888.
72. Senok AC, Ismaeel AY, Botta GA. 2005. Probiotics: facts and myths. Clin Microbiol Infect. 11:958–966.
73. Shao Y, Zhang W, Guo H, Pan L, Zhang H, Sun T. 2015. Comparative studies on antibiotic resistance in Lactobacillus casei and Lactobacillus plantarum. Food Control. 50:250–258.
74. Sharpe ME, Hill LR, Lapage SP. 1973. Pathogenic lactobacilli. J Med Microbiol. 6:281–286.
75. Sherid M, Samo S, Sulaiman S, Husein H, Sifuentes H, Sridhar S. 2016. Liver abscess and bacteremia caused by lactobacillus: role of probiotics? Case report and review of the literature. BMC Gastroenterol. 16:138.
76. Sherman ME, Albrecht M, DeGirolami PC, Kirkley SA, Wolf B, Eliopoulos GM, Rohrer RJ, Monaco AP. 1987. An unusual case of splenic abscess and sepsis in an immunocompromised host. Am J Clin Pathol. 88:659–662.
77. Snydman DR. 2008. The safety of probiotics. Clin Infect Dis. 46:S 104–111.
78. Sriskandan S, Lacey S, Fisher L. 1993. Isolation of vancomycin-resistant lactobacilli from three neutropenic patients with pneumonia. Eur J Clin Microbiol Infect Dis. 12:649–650.
79. Sybesma W, Molenar D, van Ijcken W, Venema K, Kort R. 2013. Genome instability in Lactobacillus rhamnosus GG. Appl Environ Microbiol. 79:2233–2239.
80. Tan KP, Yang M, Ito S. 2007. Activation of nuclear factor (ery-throid-2 like) factor 2 by toxic bile acids provokes adaptive defense responses to enhance cell survival at the emergence of oxidative stress. Mol Pharmacol. 72:1380–1390.
81. Tan LT-H, Chan K-G, Lee L-H, Goh B-H. 2016. Streptomyces bacteria as potential probiotics in aquaculture. Front Microbiol. 7:79.
82. Temmerman R, Pot B, Huys G, Swings J. 2002. Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int J Food Microbiol. 81:1–10.
83. Teuber M, Meile L, Schwarz F. 1999. Acquired antibiotic resistance in lactic acid bacteria from food. Antoine Van Leeuwenhoek. 76:115–137.
84. Thompson C, McCarter YS, Krause PJ, Herson VC. 2001. Lactobacillus acidophilus sepsis in a neonate. J Perinatol. 21:258–260.
85. Tissier H. 1906. Treatment of intestinal infections using bacterial flora of the intestine. Crit Rev Soc Biol. 60:359–361.
86. Tsai Y-T, Cheng P-C, Pan T-M. 2012. The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits. Appl Microbiol Biotechnol. 96:853–862.
87. Tynkkynen S, Singh KV, Varmanen P. 1998. Vancomycin resistance factor of Lactobacillus rhamnosus GG in relation to entero-coccal vancomycin resistance (van) genes. Int J Food Microbiol. 41:195–204.
88. Vahabnezhad E, Mochon AB, Wozniak LJ, Ziring DA. 2013. Lactobacillus bacteremia associated with pobiotic use in a pediatric patient with ulcerative colitis. J Clin Gastroenterol. 47: 437–439.
89. Van den Nieuwboer M, Brummer RJ, Guarner F, Cabana M, Morelli L, Claassen E. 2015. Safety of probiotics and synbiotics in children under 18 years of age. Benef Microbes. 6:615–630.
90. Van den Nieuwboer M, Claassen E, Morelli L, Guarner F, Brummer RJ. 2014. Probiotic and synbiotic safety in infants under two years of age. Benef Microbes. 5:45–60.
91. Van Leeuwen PAM, Boermeester MA, Houdijk APJ, Fer-werda ChC, Cuesta MA, Meyer S. 1994. Clinical significance of translocation. Gut. 35(Suppl):S28–S34.
92. Vankerckhoven V, Huys G, Vancanneyt M, Vael C, Klare I, Romond MB, Enteza JM, Moreillon P, Wind RD, Knol J, et al. 2008. Biosafety assessment of probiotics used for human consumption: recommendations from the EU-PROSAFE project. Trend Food Sci Tech. 19:102–114.
93. Venugopalan V, Shriner KA, Wong-Beringer A. 2010. Regulatory oversight and safety of probiotic use. Emerging Infect Dis. 11:1661–1665.
94. Vitetta L, Coulson S, Thomsen M, Nguyen T, Hall S. 2017. Probiotics, D-lactic acidosis, oxidative stress and strain specificity. Gut Microb. 8:311–322.
95. Zawistowska-Rojek A, Zaręba T, Mrówka A, Tyski S. 2016. Assessment of the microbiological status of probiotic products. Pol J Microb. 65:97–104.
96. Zheng M, Zhang R, Tian X, Zhou X, Pan X, Wong A. 2017. Assessing the risk of probiotic dietary supplements in the context of antibiotic resistance. Front Microbiol. 8:908.