Safety evaluation of two bacterial strains used in asian probiotic products

Canadian Journal of Microbiology

Volumn 54, Issue 5, 2008, Pages 391-400

  Tompkins, Thomas A ^a   Hagen, Karen E ^a   Wallace, Timothy D ^a   Fillion Forté, Valerie ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

Antibiotic resistance; Bacillus; Enterococcus; Safety; Toxins; Virulence factors

Indexed keywords

ANTIBIOTICS; FOOD PROCESSING; RISK ANALYSIS; TOXICITY;

BACTERIAL STRAINS; PROBIOTIC PRODUCTS;

BACTERIA;

ENTEROTOXIN; PROBIOTIC AGENT; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOTECHNOLOGY; DRUG; FOOD SAFETY; GUIDELINE; MOLECULAR ANALYSIS; PROBIOTICS; RISK FACTOR; TOXICITY TEST; VIRULENCE;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; ASIA; BACILLUS SUBTILIS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; ENTEROCOCCUS FAECIUM; EPITHELIUM CELL; EUROPE; FEMALE; HUMAN; HUMAN CELL; MALE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; TOXICITY TESTING;

ANIMALS; ANTI-BACTERIAL AGENTS; ASIA; BACILLUS SUBTILIS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BACTERIAL TOXINS; CONSUMER PRODUCT SAFETY; DNA, BACTERIAL; DNA, RIBOSOMAL; ENTEROCOCCUS FAECIUM; EPITHELIAL CELLS; FEMALE; FOOD MICROBIOLOGY; GRAM-POSITIVE BACTERIAL INFECTIONS; HT29 CELLS; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PLASMIDS; PROBIOTICS; RATS; RATS, SPRAGUE-DAWLEY; RNA, RIBOSOMAL, 16S; VIRULENCE FACTORS;

ASIA; EURASIA; EUROPE;

BACILLUS (BACTERIUM); BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ENTEROCOCCUS; ENTEROCOCCUS FAECIUM; RATTUS;

EID: 43949144913     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W08-022     Document Type: Article

References (55)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402. doi:10.1093/nar/25.17.3389. PMID:9254694.
2. Andersson, M.A., Mikkola, R., Helin, J., Andersson, M.C., and Salkinoja-Salonen, M. 1998. A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Appl. Environ. Microbiol. 64: 1338-1343. PMID: 9546170.
3. Apetroaie, C., Andersson, M.A., Sproer, C., Tsitko, I., Shaheen, R., Jaaskelainen, E.L., et al. 2005. Cereulide-producing strains of Bacillus cereus show diversity. Arch. Microbiol. 184: 141-151. doi:10.1007/s00203-005-0032-1. PMID:16195898.
4. Beattie, S.H., and Williams, A.G. 1999. Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay. Lett. Appl. Microbiol. 28: 221-225. doi:10.1046/j.1365-2672.1999.00498.x. PMID:10196773.
5. Becquet, P. 2003. EU assessment of enterococci as feed additives. Int. J. Food Microbiol. 88: 247-254. doi:10.1016/S0168-1605(03)00187-9. PMID:14596997.
6. Chen, X., and Wu, X.-J. 2005. A clinical study of Medilac-vita combined with loperamide hydrochloride for the treatment of infantile diarrhea. Acta Med. Sinicae, 18: 164-165.
7. CLSI. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-seventh edition. M7-A7 [online]. Available from http://www.clsi.org/source/orders/free/m11a7.pdf [accessed 1 November 2007].
8. CLSI. 2007. Performance standards for antimicrobial susceptibility testing; seventh informational supplement. M100-S17.
9. Czerucka, D., Dahan, S., Mograbi, B., Rossi, B., and Rampal, P. 2000. Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli-infected T84 cells. Infect. Immun. 68: 5998-6004. doi:10.1128/IAI.68.10.5998-6004.2000. PMID:10992512.
10. Duc le, H., Hong, H.A., Barbosa, T.M., Henriques, A.O., and Cutting, S.M. 2004. Characterization of Bacillus probiotics available for human use. Appl. Environ. Microbiol. 70: 2161-2171. doi:10.1128/AEM.67.4.1628-1635. 2001. PMID:11282615.
11. Eaton, T.J., and Gasson, M.J. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67: 1628-1635. doi:10.1128/AEM.67.4.1628-1635.2001. PMID:11282615.
12. Eaton, T.J., and Gasson, M.J. 2002. A variant enterococcal surface protein Esp(fm) in Enterococcus faecium; distribution among food, commensal, medical, and environmental isolates. FEMS Microbiol. Lett. 216: 269-275. doi:10.1111/j.1574-6968.2002.tb11446.x. PMID:12435513.
13. EFSA. 2005. Opinion of the scientific panel on additives and products or substances used in animal feed on a request from the commission on the safety of the product Lactiferm for chickens for fattening for use as a feed additive. The EFSA Journal, 207: 1-6.
14. EFSA. 2006. Opinion of the scientific panel on additives and products or substances used in animal feed (FEEDAP) on the safety and efficacy of the product "Biomin IMB 52" a preparation of Enterococcus faecium as a feed additive for chickens for fattening in accordance with regulation (EC) No. 1831/2003. The EFSA Journal, 335: 1-10.
15. EFSA. 2007. Opinion of the scientific committee on a request from EFSA on the introduction of a qualified presumption of safety (QPS) approach for the assessment of selected microorganisms referred to EFSA. The EFSA Journal, 587: 1-16.
16. Ehling-Schulz, M., Vukov, N., Schulz, A., Shaheen, R., Andersson, M., Martlbauer, E., and Scherer, S. 2005a. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl. Environ. Microbiol. 71: 105-113. doi:10.1128/AEM. 71.1.105-113.2005. PMID:15640177.
17. Ehling-Schulz, M., Svensson, B., Guinebretiere, M.H., Lindback, T., Andersson, M., Schulz, A., et al. 2005b. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology (Reading), 151: 183-197. doi:10.1099/mic.0.27607-0. PMID:15632437.
18. Ehling-Schulz, M., Guinebretiere, M.H., Monthan, A., Berge, O., Fricker, M., and Svensson, B. 2006. Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiol. Lett. 260: 232-240. doi:10.1111/j.1574-6968.2006.00320.x. PMID:16842349.
19. EUCAST. 2007. Antimicrobial wild type distributions of microorganisms. Available from http://217.70.33.99/Eucast2/ [accessed 1 November 2007].
20. European Union. 1986. 86/609/EEC: The approximation of laws, regulations and administrative provisions of the member states regarding the protection of animals used for experimental and other scientificpurposes[online]. Availablefromhttp://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CELEX: 31986L0609:EN:NOT [accessed24November1986].
21. FAO and WHO. 2002. Guidelines for the evaluation of probiotics in Food. Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food, London, Ontario, Canada, 30 April and 1 May 2002.
22. FEEDAP. 2005. Opinion of the scientific panel on additives and products or substances used in animal feed on the updating of the criteria used in assessment of bacteria for resistance to antibiotics of human or veterinary importance. The EFSA Journal, 223: 1-12.
23. Franz, C.M., Stiles, M.E., Schleifer, K.H., and Holzapfel, W.H. 2003. Enterococci in foods - a conundrum for food safety. Int. J. Food Microbiol. 88: 105-122. doi:10.1016/S0168-1605(03) 00174-0. PMID:14596984.
24. From, C., Pukall, R., Schumann, P., Hormazabal, V., and Granum, P.E. 2005. Toxin-producing ability among Bacillus spp. outside the Bacillus cereus group. Appl. Environ. Microbiol. 71: 1178-1183. doi:10.1128/AEM.71.3.1178-1183.2005. PMID:15746316.
25. Gopal, P.K., Prasad, J., Smart, J., and Gill, H.S. 2001. In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int. J. Food Microbiol. 67: 207-216. doi:10.1016/S0168-1605(01)00440-8. PMID: 11518430.
26. Green, D.H., Wakeley, P.R., Page, A., Barnes, A., Baccigalupi, L., Ricca, E., and Cutting, S.M. 1999. Characterization of two Bacillus probiotics. Appl. Environ. Microbiol. 65: 4288-4291. PMID:10473456.
27. Guan, L.L., Hagen, K.E., Tannock, G.W., Korver, D.R., Fasenko, G.M., and Allison, G.E. 2003. Detection and identification of Lactobacillus species in crops of broilers of different ages by using PCR-denaturing gradient gel electrophoresis and amplified ribosomal DNA restriction. Appl. Environ. Microbiol. 69: 6750-6757. doi:10.1128/AEM.69.11.6750-6757.2003. PMID:14602636.
28. Hoa, N.T., Baccigalupi, L., Huxham, A., Smertenko, A., Van, P.H., Ammendola, S., Ricca, E., and Cutting, A.S. 2000. Characterization of Bacillus species used for oral bacteriotherapy and bacterioprophylaxis of gastrointestinal disorders. Appl. Environ. Microbiol. 66: 5241-5247. doi:10.1128/AEM.66.12.5241-5247. 2000. PMID:11097897.
29. Hong, H.A., Duc le, H., and Cutting, S.M. 2005. The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 29: 813-835. doi:10.1016/j.femsre.2004.12.001. PMID:16102604.
30. Huycke, M.M., Sahm, D.F., and Gilmore, M.S. 1998. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4: 239-249. PMID: 9621194.
31. Jenkins, B., Holsten, S., Bengmark, S., and Martindale, R. 2005. Probiotics: a practical review of their role in specific clinical scenarios. Nutr. Clin. Pract. 20: 262-270. PMID:16207661.
32. Johnson-Henry, K.C., Hagen, K.E., Gordonpour, M., Tompkins, T.A., and Sherman, P.M. 2007. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell. Microbiol. 9: 356-367. doi:10.1111/j.1462-5822.2006.00791.x. PMID: 16925785.
33. Klare, I., Konstabel, C., Mueller-Bertling, S., Werner, G., Strommenger, B., Kettlitz, C., et al. 2005. Spread of ampicillin/vancomycin-resistant Enterococcus faecium of the epidemic-virulent clonal complex-17 carrying the genes esp and hyl in German hospitals. Eur. J. Clin. Microbiol. Infect. Dis. 24: 815-825. doi:10.1007/s10096-005-0056-0. PMID:16374593.
34. Koehler, T.M., and Thorne, C.B. 1987. Bacillus subtilis (natto) plasmid pLS20 mediates interspecies plasmid transfer. J. Bacteriol. 169: 5271-5278. PMID:3117774.
35. Leavis, H.L., Willems, R.J., Top, J., Spalburg, E., Mascini, E.M., Fluit, A.C., et al. 2003. Epidemic and nonepidemic multidrug-resistant Enterococcus faecium. Emerg. Infect. Dis. 9: 1108-1115. PMID:14519248.
36. Leavis, H., Top, J., Shankar, N., Borgen, K., Bonten, M., van Embden, J., and Willems, R.J. 2004. A novel putative enterococcal pathogenicity island linked to the esp virulence gene of Enterococcus faecium and associated with epidemicity. J. Bacteriol. 186: 672-682. doi:10.1128/JB.186.3.672-682.2004. PMID:14729692.
37. Mercenier, A., Pavan, S., and Pot, B. 2003. Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr. Pharm. Des. 9: 175-191. doi:10.2174/1381612033392224. PMID:12570667.
38. Naser, S.M., Hagen, K.E., Vancanneyt, M., Cleenwerck, I., Swings, J., Tompkins, T.A. 2006. Lactobacillus suntoryeus Cachat and Priest 2005 is a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (Approved Lists 1980). Int. J. Syst. Evol. Microbiol., 56(Pt 2):355-360. doi:10.2174/1381612033392224. PMID:12570667.
39. Pultz, N.J., Shankar, N., Baghdayan, A.S., and Donskey, C.J. 2005. Enterococcal surface protein Esp does not facilitate intestinal colonization or translocation of Enterococcus faecalis in clindamycin-treated mice. FEMS Microbiol. Lett. 242: 217-219. doi:10.1016/j.femsle.2004.11.006. PMID:15621440.
40. Requena, T., Burton, J., Matsuki, T., Munro, K., Simon, M.A., Tanaka, R., Watanabe, K., and Tannock, G.W. 2002. Identification, detection, and enumeration of human Bifidobacterium species by PCR targeting the transaldolase gene. Appl. Environ. Microbiol. 68: 2420-2427. doi:10.1128/AEM.68.5.2420-2427. 2002. PMID:11976117.
41. Reviriego, C., Eaton, T., Martin, R., Jimenez, E., Fernandez, L., Gasson, M.J., and Rodriguez, J.M. 2005. Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. J. Hum. Lact. 21: 131-137. doi:10.1177/0890334405275394. PMID:15886339.
42. Rowan, N.J., Deans, K., Anderson, J.G., Gemmell, C.G., Hunter, I.S., and Chaithong, T. 2001. Putative virulence factor expression by clinical and food isolates of Bacillus spp. after growth in reconstituted infant milk formulae. Appl. Environ. Microbiol. 67: 3873-3881. doi:10.1128/AEM.67.9. 3873-3881.2001. PMID: 11525980.
43. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
44. Sanders, M.E., Morelli, L., and Tompkins, T.A. 2003. Sporeformers as human probiotics: Bacillus Sporolactobacillus, and Brevibacillus. Compre. Rev. Food Sci. Food Saf.2: 101-110. doi:10.1111/j.1541-4337.2003. tb00017.x.
45. Schoeni, J.L., and Wong, A.C. 2005. Bacillus cereus food poisoning and its toxins. J. Food Prot. 68: 636-648. PMID:15771198.
46. Shankar, V., Baghdayan, A.S., Huycke, M.M., Lindahl, G., and Gilmore, M.S. 1999. Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect. Immun. 67: 193-200. PMID:9864215.
47. Shankar, N., Lockatell, C.V., Baghdayan, A.S., Drachenberg, C., Gilmore, M.S., and Johnson, D.E. 2001. Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect. Immun. 69: 4366-4372. doi:10.1128/IAI.69.7.4366-4372.2001. PMID:11401975.
48. Shankar, N., Baghdayan, A.S., and Gilmore, M.S. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature, 417: 746-750. doi:10.1038/nature00802. PMID:12066186.
49. Singh, K.V., Coque, T.M., Weinstock, G.M., and Murray, B.E. 1998. In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol. Med. Microbiol. 21: 323-331. PMID:9753005.
50. Sorokulova, I.B., Pinchuk, I.V., Denayrolles, M., Osipova, I.G., Huang, J.M., Cutting, S.M., and Urdaci, M.C. 2008. The safety of two Bacillus probiotic strains for human use. Dig. Dis. Sci. 53: 954-963. doi:10.1007/s10620-007-9959-1.
51. Spinosa, M.R., Wallet, F., Courcol, R.J., and Oggioni, M.R. 2000. The trouble in tracing opportunistic pathogens: cholangitis due to Bacillus in a French hospital caused by a strain related to an Italian probiotic? Microb. Ecol. Health Dis. 12: 99-101. doi:10.1080/089106000435491.
52. Tannock, G.W., Tilsala-Timisjarvi, A., Rodtong, S., Ng, J., Munro, K., and Alatossava, T. 1999. Identification of Lactobacillus isolates from the gastrointestinal tract, silage, and yoghurt by 16S-23S rRNA gene intergenic spacer region sequence comparisons. Appl. Environ. Microbiol. 65: 4264-4267. PMID:10473450.
53. Walter, J., Tannock, G.W., Tilsala-Timisjarvi, A., Rodtong, S., Loach, D.M., Munro, K., and Alatossava, T. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl. Environ. Microbiol. 66: 297-303. PMID:10618239.
54. Wang, H.J., Liang, X.M., Yu, Z.L., Liu, X.G., Yu, Y.Y., and Cheng, L.F. 2004. Efficacy and safety of Bacillus subtilis and Enterococcus faecium in treatment of acute and chronic diarrhea. Chin. J. New Drugs, 13: 452-455.
55. Yang, H. 1999. A Report of Medilac-Vita in the treatment of 40 cases of infantile constipation. Chin. J. Contemp. Pediatr., 1: 188.