Advertisement

Assessment of the Risk of Probiotics in Terms of the Food Safety and Human Health

  • Selin KalkanEmail author
  • Zerrin Erginkaya
  • Emel Ünal Turhan
  • Gözde Konuray
Chapter

Abstract

Probiotics are often referred to as microorganisms (bacteria or yeasts) that generally provide health benefits. There is great interest in probiotics for various medical reasons and millions of people around the world consume probiotic microorganisms daily with the perception that it is beneficial for health. Members of the genus Lactococcus and Lactobacillus, Streptococcus, Enterococcus strains, and some other LAB strains are generally accepted as safe (GRAS) status, although they contain some opportunistic pathogens. In addition, some of the spore forming bacteria have been researched and used as probiotics. However, nowadays theoretical concerns and side effects are discussed with regard to the safety of probiotics. Systemic infections, the risk of harmful metabolic activities, risk of adjuvant side effects, immunomodulation and gene transfer risk are among the theoretical concerns discussed. The most common side effects of probiotic microorganisms include gastrointestinal disorders such as nausea, diarrhea, bloating, abdominal pain and dyspepsia. Other side effects include respiratory tract infections, abscess, allergic reactions and severe medical conditions such as sepsis, endocarditis and fungemia. The safety of probiotics is related to the potential vulnerability of the consumer or the patient, the dose of use, duration of consumption and the frequency of consumption. The significance of negative probiotic effects will be better understood by understanding of the probiotic interaction mechanisms with host and colonizing microbes. In this chapter, the evaluation of the risk associated with the consumption of probiotic products has been discussed, based on epidemiological data and infected cases.

Keywords

Probiotics Food safety Risk assessment Health 

References

  1. Aakra Å, Nyquist L, Snipen L et al (2007) Survey of genomic diversity among Enterococcus faecalis strains by microarray-based comparative genomic hybridisation. Appl Environ Microbiol 73(7):2207–2217CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abriouel H, Benomar N, Molinos AC et al (2008) Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water, soil, and clinical samples. Int J Food Microbiol 123(1-2):38–49CrossRefPubMedGoogle Scholar
  3. Adams MR, Marteau P (1995) On the safety of lactic acid bacteria from food. Int J Food Microbiol 27(2-3):263–264CrossRefPubMedGoogle Scholar
  4. Ahn C, Collins-Thompson D, Duncan C et al (1992) Mobilization and location of the genetic determinant of chloramphenicol resistance from Lactobacillus plantarum caTC2R. Plasmid 27(3):169–176CrossRefPubMedGoogle Scholar
  5. Ammor MS, Florez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24(6):559–570CrossRefPubMedGoogle Scholar
  6. Antony S, Stratton CW, Dummer JS (1996) Lactobacillus bacteremia: description of the clinical course in adult patients without endocarditis. Clin Infect Dis 23(4):773–778CrossRefPubMedGoogle Scholar
  7. Asahara T, Takahashi M, Nomoto K et al (2003) Assessment of safety of lactobacillus strains based on resistance to host innate defense mechanisms. Clin Diagn Lab Immunol 10(1):169–173PubMedPubMedCentralGoogle Scholar
  8. Bassetti S, Frei R, Zimmerli W (1998) Fungemia with Saccharomyces cerevisiae after treatment with Saccharomyces boulardii. Am J Med 105(1):71–72CrossRefPubMedGoogle Scholar
  9. Berg RD, Garlington AW (1979) Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in the gnotobiotic Mouse model. Infect Immun 23(2):403–411PubMedPubMedCentralGoogle Scholar
  10. Bongaerts G, Bakkeren J, Severijnen R et al (2000) Lactobacilli and acidosis in children with short small bowel. J Pediatr Gastroenterol Nutr 30(3):288–293CrossRefPubMedGoogle Scholar
  11. Borriello SP, Hammes WP, Holzapfel W et al (2003) Safety of probiotics that contain lactobacilli or bifidobacterial. Clin Infect Dis 36(6):775–780CrossRefPubMedGoogle Scholar
  12. Boyle RJ, Robins-Browne RM, Tang ML (2006) Probiotic use in clinical practice: what are the risks? Am J Clin Nutr 83(6):1256–1264CrossRefPubMedGoogle Scholar
  13. Bozkurt H, Aslım B (2004) İmmobilizasyonun Probiyotik Kültürlerde Kullanımı. Orlab On-Line Mikrobiyoloji Dergisi 2(7):01–14Google Scholar
  14. Cannon JP, Lee TA, Bolanos JT et al (2005) Pathogenic relevance of Lactobacillus: a retrospective review of over 200 cases. Eur J Clin Microbiol Infect Dis 24(1):31–40CrossRefPubMedGoogle Scholar
  15. Cassone M, Serra P, Mondello F et al (2003) Outbreak of Saccharomyces cerevisiae subtype boulardii fungemia in patients neighboring those treated with a probiotic preparation of the organism. J Clin Microbiol 41(11):5340–5343CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cesaro S, Chinello P, Rossi L et al (2000) Saccharomyces cerevisiae fungemia in a neutropenic patient treated with Saccharomyces boulardii. Support Care Cancer 8(6):504–505CrossRefPubMedGoogle Scholar
  17. Ceyhan N, Alıç H (2012) Bağırsak Mikroflorası ve Probiyotikler. Türk Bilimsel Derlemeler Dergisi 5(1):107–113Google Scholar
  18. Ciffo F (1984) Determination of the spectrum of antibiotic resistance of the Bacillus subtilis strains of Enterogermina. Chemioterapia 3(1):45–52PubMedGoogle Scholar
  19. Clancy R (2003) Immunobiotics and the probiotic evolution. FEMS Immunol Med Microbiol 38(1):9–12CrossRefPubMedGoogle Scholar
  20. Connolly E, Abrahamsson T, Bjorksten B (2005) Safety of D(-)-lactic acid producing bacteria in the human infant. J Pediatr Gastroenterol Nutr 41(4):489–492CrossRefPubMedGoogle Scholar
  21. Çoşkun T (2006) Pro-, Pre- ve Sinbiyotikler. Çocuk Sağlığı ve Hastalıkları Dergisi 49(2):128–148Google Scholar
  22. Cunningham-Rundles S, Ahrné S, Bengmark S et al (2000) Probiotics and immune response. Am J Gastroenterol 95(1):S22–S25CrossRefPubMedGoogle Scholar
  23. De Boer AS, Diderichsen B (1991) On the safety of Bacillus subtilis and B. amyloliquefaciens: a review. Appl Microbiol Biotechnol 36:1–4CrossRefPubMedGoogle Scholar
  24. De Groote MA, Frank DN, Dowell E et al (2005) Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Pediatr Infect Dis J 24(3):278–280CrossRefPubMedGoogle Scholar
  25. 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(9):2912–2919CrossRefGoogle Scholar
  26. Dewan S, Tamang JP (2007) Dominant lactic acid bacteria and their technological properties isolated from the himalayan ethnic fermented milk products. Antonie Van Leeuwenhoek 92(3):343–352CrossRefPubMedGoogle Scholar
  27. Domann E, Hain T, Ghai R et al (2007) Comparative genomic analysis for the presence of potential enterococcal virulence factors in the probiotic Enterococcus faecalis strain Symbioflor 1. Int J Med Microbiol 297(7-8):533–539CrossRefPubMedGoogle Scholar
  28. Donohue DC, Salminen S (1996) Safety of probiotic bacteria. Asia Pac J Clin Nutr 5:25–28PubMedGoogle Scholar
  29. Duc LH, Dong TC, Logan NA et al (2005) Cases of emesis associated with bacterial contamination of an infant breakfast cereal product. Int J Food Microbiol 102(2):245–251CrossRefGoogle Scholar
  30. Duffy LC (2000) Interactions mediating bacterial translocation in the immature intestine. J Nutr 130(2):432–436CrossRefGoogle Scholar
  31. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67(4):1628–1635CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ebners S, Smug LN, Kneifel W et al (2014) Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol 20(43):16095–16100CrossRefGoogle Scholar
  33. FAO/WHO (2001) Food and Agriculture Organization/World Health Organization. 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. Available from http://www.fao.org/es/ESN/food/foodandfood_probio_en.stm. Accessed 1 July 2003Google Scholar
  34. FAO/WHO. (2002) Food and Agriculture Organization/World Health Organization. Guidelines for the evaluation of probiotics in foods, report of a joint FAO/WHO working group, London, Ontario, Canada, April 30 and May 1 2002. Available from ftp://ftp.fao.org/es/esn/food/wgreport2.pdfGoogle Scholar
  35. Franz CMAP, Muscholl-Silberhorn AB, Yousif NMK (2001) Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol 67(9):4385–4389CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fredenucci I, Chomarat M, Boucaud C et al (1998) Saccharomyces boulardii fungemia in a patient receiving Ultra-levure therapy. Clin Infect Dis 27(1):222–223CrossRefPubMedGoogle Scholar
  37. Friedman G (2005) Probiotics, prebiotics, and commensal bacteria: perspectives and clinical applications in gastroenterology. Gastroenterol Clin North Am 34(3):13–16CrossRefGoogle Scholar
  38. From C, Pukall R, Schumann P et al (2005) Toxin-producing ability among Bacillus spp. outside the Bacillus cereus group. Appl Environ Microbiol 71(3):1178–1183CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gallemore GH, Mohon RT, Ferguson DA (1995) Lactobacillus fermentum endocarditis involving a native mitral valve. J Tenn Med Assoc 88(8):306–308PubMedGoogle Scholar
  40. Gasser F (1994) Safety of lactic-acid bacteria and their occurrence in human clinical infections. Bull Inst Pasteur 92:45–67Google Scholar
  41. Gevers D, Danielsen M, Huys G et al (2003) Molecular characterization of tet(M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol 69(2):1270–1275CrossRefPubMedPubMedCentralGoogle Scholar
  42. Gismondo MR, Drago L, Lombardi A (1999) Review of probiotics available to modify gastrointestinal flora. Int J Antimicrob Agents 12(4):287–292CrossRefPubMedGoogle Scholar
  43. Gönülateş N (2008) Kefirin insanlar üzerindeki immünomodülatör etkilerinin araştırılması. (Doctoral dissertation, SDÜ Tıp Fakültesi)Google Scholar
  44. Granum PE (2002) Bacillus cereus and food poisoning. In: Berkeley R, Heyndrickx M, Logan NA, de Vos P (eds) Applications and systematics of bacillus and relatives. Blackwell Science, Oxford, pp 37–46Google Scholar
  45. Granum PE, Lund T (1997) Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett 157(2):223–228CrossRefPubMedGoogle Scholar
  46. Green DH, Wakeley PR, Page A et al (1999) Characterization of two Bacillus probiotics. Appl Environ Microbiol 65(9):4288–4291PubMedPubMedCentralGoogle Scholar
  47. Guarner F, Schaafsma GJ (1998) Probiotics. Int J Food Microbiol 39(3):237–238CrossRefPubMedGoogle Scholar
  48. Guinebretiere MH, Broussolle V, Nguyen-The C (2002) Enterotoxigenic profiles of food-poisoning and food borne Bacillus cereus strains. J Clin Microbiol 40:3053–3056CrossRefPubMedPubMedCentralGoogle Scholar
  49. Gülmez M, Güven A (2002) Probiyotik prebiyotik ve sinbiyotikler. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 8:83–89Google Scholar
  50. Hennequin C, Kauffmann-Lacroix C, Jobert A et al (2000) Possible role of catheters in Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect Dis 19(1):16–20CrossRefPubMedGoogle Scholar
  51. Henriksson A, Borody T, Clancy R (2005) Probiotics under the regulatory microscope. Expert Opin Drug Saf 4(6):1135–1143CrossRefPubMedGoogle Scholar
  52. Herreros MA, Sandoval H, González L et al (2005) Antimicrobial activity and antibiotic resistance of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese). Food Microbiol 22(5):455–459CrossRefGoogle Scholar
  53. Hong HA, Duc LH, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29(4):813–835CrossRefPubMedGoogle Scholar
  54. Huang Y, Kotula L, Adams MC (2003) The in-vivo assessment of safety and gastrointestinal survival of an orally administered novel probiotic, Propionibacterium jensenii 702, in a male Wistar rat model. Food Chem Toxicol 41(12):1781–1787CrossRefPubMedGoogle Scholar
  55. Husni RN, Gordon SM, Washington JA et al (1997) Lactobacillus bacteremia and endocarditis: review of 45 cases. Clin Infect Dis 25(5):1048–1055CrossRefPubMedGoogle Scholar
  56. Ishibashi N, Yamazaki S (2001) Probiotics and safety. Am J Clin Nutr 73(2):465–470CrossRefGoogle Scholar
  57. Johnson AP (1994) The pathogenicity of enterococci. Int J Antimicrob Agents 33(6):1083–1089Google Scholar
  58. Kalima P, Masterton RG, Roddie PH (1996) Lactobacillus rhamnosus infection in a child following bone marrow transplant. J Infect 32(2):165–167CrossRefPubMedGoogle Scholar
  59. Kayser FH (2003) Safety aspects of enterococci from the medical point of view. Int J Food Microbiol 88(2-3):255–262CrossRefPubMedGoogle Scholar
  60. Klein G, Hallmann C, Casas IA (2000) Exclusion of vanA, vanB and vanC type glycopeptide resistance in strains of Lactobacillus reuteri and Lactobacillus rhamnosus used as probiotics by polymerase chain reaction and hybridization methods. J Appl Microbiol 89:815–824CrossRefPubMedGoogle Scholar
  61. Koehler TM, Thorne CB (1987) Bacillus subtilis (natto) plasmid pLS20 mediates interspecies plasmid transfer. J Bacteriol 169(11):5271–5278CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kramer JM, Turnbull PCB, Munshi G et al (1982) Identification and characterization of Bacillus cereus and other Bacillus species associated with foods and food poisoning. In: Corry JEL, Roberts D, And Skinner FA (eds) Isolation and identification methods for food poisoning organisms. Academic Press, London, pp 261–286Google Scholar
  63. Kunz AN, Noel JM, Fairchok MP (2004) Two cases of Lactobacillus bacteremia during probiotic treatment of short gut syndrome. J Pediatr Gastroenterol Nutr 38(4):457–458CrossRefPubMedGoogle Scholar
  64. Land MH, Rouster-Stevens K, Woods CR et al (2005) Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115(1):178–181CrossRefPubMedGoogle Scholar
  65. Landman D, Quale JM (1997) Management of infections due to resistant enterococci: a review of therapeutic options. J Antimicrob Chemother 40:161–170CrossRefPubMedGoogle Scholar
  66. Leclercq R (1997) Enterococci acquire new kinds of resistance. Clin Infect Dis 24(Suppl.1):80–84CrossRefGoogle Scholar
  67. Lee YK, Salminen S (2009) Handbook of probiotics and prebiotics. John Wiley & Sons, New YorkGoogle Scholar
  68. Lepage E, Brinster S, Caroin C et al (2006) Comparative genomic hybridization analysis of Enterococcus faecalis: identification of genes absent from food strains. J Bacteriol 188(9):6858–6868CrossRefPubMedPubMedCentralGoogle Scholar
  69. Lherm T, Monet C, Nougiere B et al (2002) Seven cases of fungemia with Saccharomyces boulardii in critically ill patients. Intensive Care Med 28(6):797–801CrossRefPubMedGoogle Scholar
  70. Lin CF, Fung ZF, Wu CL et al (1996) Molecular characterization of a plasmid-borne (pTC82) chloramphenicol resistance determinant (cat-TC) from Lactobacillus reuteri G4. Plasmid 36(2):116–124CrossRefPubMedGoogle Scholar
  71. Liong MT, Shah NP (2005) Bile salt deconjugation and BSH activity of five bifidobacterial strains and their cholesterol co-precipitating properties. Food Res Int 38(2):135–142CrossRefGoogle Scholar
  72. Logan NA (2004) Safety of aerobic endospore-forming bacteria. In: Ricca E, Henriques AO, Cutting SM (eds) Bacterial spore formers: probiotics and emerging applications. Horizon Bioscience, Norfolk, pp 93–106Google Scholar
  73. Maragkoudakis PA, Zoumpopoulou G, Miaris C et al (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16(3):189–199CrossRefGoogle Scholar
  74. Marteau P, Pochart P, Flourie B et al (1990) Effect of chronic ingestion of a fermented dairy product containing Lactobacillus acidophilus and Bifidobacterium bifidum on metabolic activities of the colonic flora in humans. Am J Clin Nutr 52(4):685–688CrossRefPubMedGoogle Scholar
  75. Martin-Platero AM, Maqueda M, Valdivia E et al (2009) Polyphasic study of microbial communities of two Spanish farmhouse goats’ milk cheeses from Sierra de Aracena. Food Microbiol 26(3):294–304CrossRefPubMedGoogle Scholar
  76. Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria-a review. Int J Food Microbiol 105(3):281–295CrossRefPubMedGoogle Scholar
  77. Mazza P, Zani F, Martelli P (1992) Studies on the antibiotic resistance of Bacillus subtilis strains used in oral bacteriotherapy. Boll Chim Farm 131(11):401–408PubMedGoogle Scholar
  78. McBride SM, Fischetti VA, LeBlanc DJ et al (2007) Genetic diversity among Enterococcus faecalis. PLoS One 2(7):e582CrossRefPubMedPubMedCentralGoogle Scholar
  79. McGowan-Spicer LL, Fedorka-Cray PJ, Frye JG et al (2008) Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food. J Food Prot 71(4):760–769CrossRefPubMedGoogle Scholar
  80. McNaught CE, Woodcock NP, MacFie J et al (2002) A prospective randomised study of the probiotic Lactobacillus plantarum 299V on indices of gut barrier function in elective surgical patients. Gut 51:827–831CrossRefPubMedPubMedCentralGoogle Scholar
  81. Metchnikoff II (2004) The prolongation of life: optimistic studies. Springer Publishing Company, New YorkGoogle Scholar
  82. Morrison D, Woodford N, Cookson B (1997) Enterococci as emerging pathogens of humans. J Appl Microbiol Symp Suppl 83:89–99CrossRefGoogle Scholar
  83. Muñoz-Atienza E, Gómez-Sala B, Araújo C et al (2013) Antimicrobial activity, antibiotic susceptibility and virulence factors of lactic acid bacteria of aquatic origin intended for use as probiotics in aquaculture. BMC Microbiol 13(1):15CrossRefPubMedPubMedCentralGoogle Scholar
  84. Murray BE (1990) The life and times of the Enterococcus. Clin Microbiol Rev 3(1):46–65CrossRefPubMedPubMedCentralGoogle Scholar
  85. Murray PR, Baron E, Jorgenson JH et al (2003) Manual of clinical microbiology. ASM Press, Washington, pp 857–869Google Scholar
  86. O’Brien J, Crittenden R, Ouwehand AC et al (1999) Safety evaluation of probiotics. Trends Food Sci Technol 10:418–424CrossRefGoogle Scholar
  87. Oggioni MR, Pozzi G, Valensin PE et al (1998) Recurrent septicemia in an immunocompromised patient due to probiotic strains of Bacillus subtilis. J Clin Microbiol 36(1):325–326PubMedPubMedCentralGoogle Scholar
  88. Olano A, Chua J, Schroeder S et al (2001) Weissella confusa (Basonym: Lactobacillus confusus) bacteremia: a case report. J Clin Microbiol 39(4):1604–1607CrossRefPubMedPubMedCentralGoogle Scholar
  89. Osipova IG, Sorokulova IB, Tereshkina NV et al (1998) Safety of bacteria of the genus Bacillus, forming the base of some probiotics. Zh Mikrobiol Epidemiol Immunobiol 6:68–70Google Scholar
  90. Otles S, Cagindi O (2003) Kefir: a probiotic dairy-composition, nutritional and therapeutic aspects. Pak J Nutr 2(2):54–59CrossRefGoogle Scholar
  91. Ouoba LII, Lei V, Jensen LB (2008) Resistance of potential probiotic lactic acid bacteria and Bifidobacteria of African and European origin to nantimicrobials: determination and transferability of the resistance genes to other bacteria. Int J Food Microbiol 121(2):217–224CrossRefPubMedGoogle Scholar
  92. 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(12):1858–1860CrossRefPubMedGoogle Scholar
  93. Özden A (2005) Gastrointestinal sistem ve probiyotik-prebiyotik-sinbiyotik. Güncel Gastroenteroloji 9(3):124–133Google Scholar
  94. Özteber M (2013) Fermente süt ürünlerinden izole edilen laktik asit bakterilerinin antibiyotik dirençliliklerinin fenotipik ve genotipik yöntemlerle belirlenmesi. Master’s thesis, Adnan Menderes Üniversitesi, Fen Bilimleri EnstitüsüGoogle Scholar
  95. Patel R, Cockerill FR, Porayko MK et al (1994) Lactobacillemia in liver transplant patients. Clin Infect Dis 18:207–212CrossRefPubMedGoogle Scholar
  96. Perapoch J, Planes AM, Querol A et al (2000) Fungemia with Saccharomyces cerevisiae in two newborns, only one of whom had been treated with ultra-levura. Eur J Clin Microbiol Infect Dis 19(6):468–470CrossRefPubMedGoogle Scholar
  97. Perdigon G, Alvarez S, Aquero G et al (1997) Interactions between lactic acid bacteria, intestinal microflora and the immune system. In: Martins MT, Zanoli Sato MI, Tiedje JM, Norton Haggler JB, Dobereiner J, Sanchez P (eds) Proceedings of the 7th International Symposium of Microbial Ecology, Santos, Brazil, pp 311–316Google Scholar
  98. Pérez-Pulido R, Abriouel H, Ben Omar N et al (2006) Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem Toxicol 44(12):2070–2077CrossRefPubMedGoogle Scholar
  99. Phelps RJ, McKillip JL (2002) Enterotoxin production in natural isolates of Bacillaceae outside the Bacillus cereus group. Appl Environ Microbiol 68(6):3147–3151CrossRefPubMedPubMedCentralGoogle Scholar
  100. Przyrembel H (2001) Consideration of possible legislation within existing regulatory frameworks. Am J Clin Nutr 73(2):471–475CrossRefGoogle Scholar
  101. Ranadheera CS, Evans CA, Adams MC (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods 8:18–25CrossRefGoogle Scholar
  102. Rautio M, Jousimies-Somer H, Kauma H et al (1999) Liver abscess due to a Lactobacillus rhamnosus strain indistinguishable from L. rhamnosus strain GG. Clin Infect Dis 28(5):1159–1160CrossRefPubMedGoogle Scholar
  103. Reid G (2002) Safety of lactobacillus strains as probiotic agents. Clin Infect Dis 35(3):349–350CrossRefPubMedGoogle Scholar
  104. Richard V, Van der Auwera P, Snoeck R et al (1988) Nosocomial bacteremia caused by Bacillus species. Eur J Clin Microbiol Infect Dis 7(6):783–785CrossRefPubMedGoogle Scholar
  105. Rodriguez AV, Baigorí MD, Alvarez S et al (2001) Phosphatidylinositol-specific phospholipase C activity in Lactobacillus rhamnosus with capacity to translocate. FEMS Microbiol Lett 204(1):33–38CrossRefPubMedGoogle Scholar
  106. Rowan NJ, Deans K, Anderson JG et al (2001) Putative virulence factor expression by clinical and food isolates of Bacillus spp. after growth in reconstituted infant milk formulae. Appl Environ Microbiol 67(9):3873–3881CrossRefPubMedPubMedCentralGoogle Scholar
  107. Ruiz-Garbajosa P, Bonten MJ, Robinson DA et al (2006) Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of evolution. J Clin Microbiol 44(6):2220–2228CrossRefPubMedPubMedCentralGoogle Scholar
  108. Ruseler-van Embden JG, van Lieshout LM, Gosselink MJ et al (1995) Inability of Lactobacillus casei strain GG, L. acidophilus, and Bifidobacterium bifidum to degrade intestinal mucus glycoproteins. Scand J Gastroenterol 30(7):675–680CrossRefPubMedGoogle Scholar
  109. Saarela M, Mogensen G, Fonden R (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84(3):197–215CrossRefPubMedGoogle Scholar
  110. Sağdıç O, Küçüköner E, Özçelik S (2004) Probiyotik ve Prebiyotiklerin Fonksiyonel Özellikleri, Atatürk Üniv. Ziraat Fak Dergisi 35(3-4):221–228Google Scholar
  111. Salminen MK (2006) Lactobacillus bacteremia, with special focus on the safety of probiotic Lactobacillus rhamnosus GG (doctoral dissertation). University of Helsinki, HelsinkiGoogle Scholar
  112. Salminen S, von Wright A, Morelli L et al (1998) Demonstration of safety of probiotics – a review. Int J Food Microbiol 44(1-2):93–106CrossRefPubMedGoogle Scholar
  113. Salminen MK, Tynkkynen S, Rautelin H et al (2002) Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis 35(10):1155–1160CrossRefPubMedGoogle Scholar
  114. Salminen MK, Rautelin H, Tynkkynen S et al (2004) Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 38(1):62–69CrossRefPubMedGoogle Scholar
  115. Salyers AA, Gupta A, Wang Y (2004) Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 12(9):412–416CrossRefPubMedGoogle Scholar
  116. Sanders ME, Morelli L, Tompkins TA (2003) Sporeformers as human probiotics: bacillus, sporolactobacillus, and brevibacillus. Compr Rev Food Sci Food Saf 2(3):101–110CrossRefGoogle Scholar
  117. Saxelin M, Chuang NH, Chassy B (1996) Lactobacilli and bacteremia in southern Finland, 1989–1992. Clin Infect Dis 22(3):564–566CrossRefPubMedGoogle Scholar
  118. SCAN (2002a) Scientific Committee on Animal Nutrition. Report of the Scientific Committee on Animal Nutrition. Opinion of the Scientific Committee on Animal Nutrition on the safety of use of Bacillus species in animal nutrition. European Commission, Health & Consumer Protection Directorate-General, BrusselsGoogle Scholar
  119. SCAN (2002b) Scientific Committee on Animal Nutrition. Report of the Scientific Committee on Animal Nutrition, Opinion of the SCAN on the criteria for assessing the safety of microorganisms resistant to antibiotics of human, clinical, and veterinary importance. European Commission Health & Consumer Protection Directorate-General, Brussels. http://europa.eu.int/comm/food/fs/sc/scan/out64_en.pdf. Accesses 1 July 2003Google Scholar
  120. Senok AC, Ismaeel AY, Botta GA (2005) Probiotics: facts and myths. Clin Microbiol Infect 11(12):958–966CrossRefPubMedGoogle Scholar
  121. Serio A, Paparella A, Chaves-López C (2007) Enterococcus populations in Pecorino Abruzzese cheese: biodiversity and safety aspects. J Food Prot 70(7):1561–1568CrossRefPubMedGoogle Scholar
  122. Shortt C (1999) The probiotic century: historical and current perspectives. Trends Food Sci Technol 10(12):411–417CrossRefGoogle Scholar
  123. Shu Q, Zhou JS, Rutherfurd KJ (1999) Probiotic lactic acid bacteria (Lactobacillus acidophilus HN017, Lactobacillus rhamnosus HN001 and Bifidobacterium lactis HN019) have no adverse effects on health of mice. Int Dairy J 9(11):831–836CrossRefGoogle Scholar
  124. Solheim M, Brekke MC, Snipen LG (2011) Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface-structure proteins in hospital-associated clonal-complex 2 Enterococcus faecalis. BMC Microbiol 11(1):3CrossRefPubMedPubMedCentralGoogle Scholar
  125. Spinosa MR, Wallet F, Courcol RJ (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(2):99–101CrossRefGoogle Scholar
  126. Sullivan A, Nord CE (2006) Probiotic lactobacilli and bacteraemia in Stockholm. Scand J Infect Dis 38(5):327–331CrossRefPubMedGoogle Scholar
  127. Snydman, D. R. (2008). The safety of probiotics. Clinical infectious diseases, 46(Supplement_2), S104–S111.Google Scholar
  128. Tall BD (2016) We are what we eat: should food microbiology take the lead on understanding how the homeostasis of the gut microbiome influences human health and disease? IAFP Annual Meeting, Des MoinesGoogle Scholar
  129. Timmerman HM, Koning CJM, Mulder L (2004) Monostrain, multistrain and multispecies probiotics - a comparison of functionality and efficacy. Int J Food Microbiol 96(3):219–233CrossRefPubMedGoogle Scholar
  130. Toprak Kavas S (2007) Probiyotik Mikroorganizmaların Gastrointestinal Sistem Uyumluluğu Ve Enterik Patojenlere Etkisi. Pamukkale Üniversitesi Tıp Fakültesi İnfeksiyon Hastalıkları ve Klinik Mikrobiyoloji Anabilim Dalı, Uzmanlık Alan TeziGoogle Scholar
  131. Tynkkynen S, Singh KV, Varmanen P (1998) Vancomycin resistance factor of Lactobacillus rhamnosus GG in relation to enterococcal vancomycin resistance (van) genes. Int J Food Microbiol 41(3):195–204CrossRefPubMedGoogle Scholar
  132. Valenzuela AS, Omar NB, Abriouel H (2008) Risk factors in enterococci isolated from foods in Morocco: determination of antimicrobial resistance and incidence of virulence traits. Food Chem Toxicol 46(8):2648–2652CrossRefPubMedGoogle Scholar
  133. Veltrop MHAM, Bancsi MJLM, Bertina RM et al (2000) Role of monocytes in experimental Staphylococcus aureus endocarditis. Infect Immun 68(8):4818–4821CrossRefPubMedPubMedCentralGoogle Scholar
  134. Vergis EN, Hayden MK, Chow JW et al (2001) Determinants of vancomycin resistance and mortality rates in enterococcal bacteremia. A prospective multicenter study. Ann Intern Med 135(7):484–492CrossRefPubMedGoogle Scholar
  135. Wassenaar TM, Klein G (2008) Safety aspects and implications of regulation of probiotic bacteria in food and food supplements. J Food Prot 71(8):1734–1741CrossRefPubMedGoogle Scholar
  136. Werner G, Coque TM, Hammerum AM et al (2008) Emergence and spread of vancomycin resistance among enterococci in Europe. Eurosurveillance 13(47):1–11Google Scholar
  137. Wheeler RT, Kupiec M, Magnelli P et al (2003) A Saccharomyces cerevisiae mutant with increased virulence. Proc Natl Acad Sci U S A 100(5):2766–2770CrossRefPubMedPubMedCentralGoogle Scholar
  138. Willems RJ, Homan W, Top J (2001) Variant esp gene as a marker of a distinct genetic lineage of vancomycin-resistant Enterococcus faecium spreading in hospitals. Lancet 357(9259):853–855CrossRefPubMedGoogle Scholar
  139. Wolf BW, Wheeler KB, Ataya DG (1998) Safety and tolerance of Lactobacillus reuteri supplementation to a population infected with the human immunodeficiency virus. Food Chem Toxicol 36(12):1085–1094CrossRefPubMedGoogle Scholar
  140. Yiğit T (2009) Süt ve Süt Ürünlerinden Probiyotik Bakterilerden İzolasyonu. Anadolu Üniversitesi,Yüksek Lisans Tezi, EskişehirGoogle Scholar
  141. Yousif NM, Dawyndt P, Abriouel H (2005) Molecular characterization, technological properties and safety aspects of enterococci from ‘Hussuwa’, an African fermented sorghum product. J Appl Microbiol 98(1):216–228CrossRefPubMedGoogle Scholar
  142. Yuksekdag ZN, Aslim B (2010) Assessment of potential probiotic-and starter properties of Pediococcus spp. isolated from Turkish-type fermented sausages (sucuk). J Microbiol Biotechnol 20(1):161–168CrossRefPubMedGoogle Scholar
  143. Zhou JS, Shu Q, Ritherford KJ et al (2000a) Acute oral toxicity and bacterial translocation studies on potentially probiotic strains of lactic acid bacteria. Food Chem Toxicol 38(2-3):153–161CrossRefPubMedGoogle Scholar
  144. Zhou JS, Shu Q, Rutherfurd KJ et al (2000b) Safety assessment of potential probiotic lactic acid bacteria strains Lactobacillus rhamnosus HN001, Lb. Acidophilus HN017 and Bifidobacterium lactis HN019 in BALB/c mice. Int J Food Microbiol 56(1):87–96CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Selin Kalkan
    • 1
    Email author
  • Zerrin Erginkaya
    • 2
  • Emel Ünal Turhan
    • 3
  • Gözde Konuray
    • 2
  1. 1.Department of Food Engineering, Faculty of EngineeringGiresun UniversityGiresunTurkey
  2. 2.Department of Food Engineering, Faculty of AgricultureCukurova UniversityAdanaTurkey
  3. 3.Department of Food Technology, Kadirli Applied Sciences SchoolOsmaniye Korkut Ata UniversityOsmaniyeTurkey

Personalised recommendations