Advertisement

The Risk of Vancomycin Resistant Enterococci Infections from Food Industry

  • Mevhibe TerkuranEmail author
  • Emel Ünal Turhan
  • Zerrin Erginkaya
Chapter

Abstract

Several works of literature research for the contribution of Antibiotic-Resistant Enterococci (ARE) and, especially Vancomycin Resistant Enterococci (VRE) which entered into the food chain has gained importance with the increasing significance of VREs in hospital infections. Various studies conducted in Europe, United States of America (USA) and the Middle East were evaluated in terms of prevalence, epidemiology and risk factors of foodborne enterococci in VRE infections. VRE epidemiology has shown some distinctions in Europe and USA. VRE was generally isolated from animals in Europe, which was connected to the extensive/massive use of “avoparcin” as a growth promoter in animal feed in the agriculture sector. Animals fed with this feed act as reservoirs of transferable vanA type resistance. On the other hand, since “avoparcin” was not used in the USA, VRE could not be isolated in animals and healthy humans. However, hospital-acquired VRE infections are more showed in the USA than in European countries. According to numerous studies, since enterococci are used as starter culture and probiotic culture, they have no relationship genetically with the strains which include vancomycin/resistant to antibiotic/or having resistance and virülence genes. In this chapter, important features of enterococci, the role of food chain for ARE especially, VRE infections in community including strategies for future solutions about the problem are summarised.

Keywords

VRE Food chain Enterococci Food industry 

References

  1. Aarestrup FM, Ahrens P, Madsen M, Pallesen LV, Poulsen RL, Westh H (1996) Glycopeptide susceptibility among Danish enterococcus faecium and Enterococcus faecalis isolates of animal and human origin and PCR identification of genes within the VanA cluster. Antimicrob Agents Chemother 40(8):1938–1940CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abeıjón MC, Medina RB, Katz MB, Silvia N, González SN (2006) Erratum: technological properties of Enterococcus faecium isolated from Ewe’s milk and cheese with importance for flavour development. Can J Microbiol 52:9–913CrossRefGoogle Scholar
  3. ACNFP (1996) Report on Enterococcus faecium, strain K77D. Report, Ergon House c/o Nobel House, 17 Smith Square, London SW1 3JR, United Kingdom: MAFF Advisory Committee on Novel Foods and ProcessesGoogle Scholar
  4. Aktaş G, Derbentli Ş (2009) Vankomisine Dirençli Enterokokların Önemive Epidemiyolojik Özellikleri. İnfeksiyon Dergisi (Turk J Emerg Med) 23(4):201–209pGoogle Scholar
  5. Alvarez CYM, Fernandez FJ, Wacher-Rodarte C, Aguılar MB, Saınz ETR, Ponce-Alqicira E (2010) Biochemical characterization of a bacteriocin-like inhibitory substance produced by Enterococcus faecium MXVK29, isolated from Mexican traditional Sausage. J Sci Food Agric 90(14):2475–281pCrossRefGoogle Scholar
  6. Askarian M, Afkhamzadeh R, Monabbati A, Daxboeck F, Assadian O (2008) Risk factors for rectal colonization with vancomycin-resistant Enterococci in Shiraz, Iran. Int J Infect Dis 12:171–175pCrossRefPubMedGoogle Scholar
  7. Atterbury RJ (2009) Bacteriophage biocontrol in animals and meat products. Microb Biotechnol 2:601–612CrossRefPubMedPubMedCentralGoogle Scholar
  8. Barakat RK, Griffiths MW, Harris LJ (2000) Isolation and characterisation of Carnobacterium, Lactococcus, and spp. from cooked, modified atmosphere packed, refrigerated, poultry meat. Int J Food Microbiol 62:83–94pCrossRefPubMedGoogle Scholar
  9. Bertrand X, Mulin B, Vıel JF, Thouverez M, Talon D (2000) Common PFGE patterns in antibiotic-resistant E. faecalis from humans and cheeses. Food Microbiol 17:543–551pCrossRefGoogle Scholar
  10. Bhardwaj A, Gupta H, Kapıla S, Kaur G, Vij S, Malik LK (2010) Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. Int J Food Microbiol 141:156–164CrossRefPubMedGoogle Scholar
  11. Boklund A, Alban L, Mortensen S, Houe H (2004) Biosecurity in 116 Danish fattening swineherds: descriptive results and factor analysis. Prev Vet Med 66:49–62pCrossRefPubMedGoogle Scholar
  12. Bonten MJ, Willems R, Weinsteın RA (2001) Vancomycin-resistant Enterococci: why are they here and where do they come from? Lancet Infect Dis 1:314–25pCrossRefPubMedGoogle Scholar
  13. Çakır I, Karahan AG, Çakmakçı L (2002) Probiyotikler ve etki mekanizmaları. Gıda Mühendisliği Dergisi 6(12):15–19Google Scholar
  14. Callaway TR, Edrington TS, Anderson RC, Harvey RB, Genovese KJ, Kennedy CN, Venn DW, Nisbet DJ (2008) Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim Health Res Rev 9:217–225pCrossRefPubMedGoogle Scholar
  15. Carasi P, Racedo SM, Jacquot C, Elie AM, Serradell ML, Urdaci MC (2017) Enterococcus durans EP1 a promising anti-inflammatory probiotic able to stimulate sIgA and to increase faecalibacteriumprausnitzii abundance. Front Immunol.  https://doi.org/10.3389/fimmu.2017.00088
  16. Castanon JI (2007) History of the use of antibiotics as growth promoters in European poultry feeds. Poult Sci 86:2466–2471CrossRefPubMedGoogle Scholar
  17. Cebrıán R, Baños A, Valdivia E, Pérez-Pulido R, Martínez-Bueno M, Maqueda M (2012) Characterization of functional, safety, and probiotic properties of Enterococcus faecalis UGRA10, a new AS-48-producer strain. Food Microbiol 30:59–67CrossRefPubMedGoogle Scholar
  18. Çetinkaya Y, Falk P, Mayhall CG (2000) Vancomycin-resistant Enterococci. Clin Microbiol Rev 13:686–707CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Dovnes FP (2003) Infection with vancomycin-resistant Staphylococcus aureus containing VanA resistance gene. N Engl J Med 348:1342–1347CrossRefPubMedGoogle Scholar
  20. Chenoweth C, Schaberg D (1990) The epidemiology of Enterococci. Eur J Clin Infect Dis 9:80–89CrossRefGoogle Scholar
  21. Çıtak S, Yücel N, Orhan S (2004) Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. Int J Dairy Technol 57:27–31CrossRefGoogle Scholar
  22. Cocconcelli PS, Cattıvellı D, Gazzola S (2003) Gene transfer of vancomycin and tetracycline resistances among Enterococcus faecalis during cheese and sausage fermentations. Int J Food Microbiol 88:315–323CrossRefPubMedGoogle Scholar
  23. Crittenden RG, Martinez NR, Playne MJ (2003) Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria. Int J Food Microbiol 80:217–222pCrossRefPubMedGoogle Scholar
  24. De Fátima Silva Lopes M, Ribeiro T, Abrantes M, Figueiredo Marques JJ, Tenreiro R, Crespo MTB (2005) Antimicrobial resistance profiles of dairy and clinical isolates and type strains of Enterococci. Int J Food Microbiol 103:191–198CrossRefPubMedGoogle Scholar
  25. De Vuyst L, Moreno MR, Revets H (2003) Screening for enterocin and detection of hemolysin and vancomycin resistance in Enterococci of different origins. Int J Food Microbiol 84:299–318CrossRefPubMedGoogle Scholar
  26. Dellit TH, Owens RC, McGowan JE Jr, Gerding DN, Weinstein RA, Burke JP, Huskins WC, Paterson DL, Fishman NO, Carpenter CF et al (2007) Infectious diseases Society of America and the Society for healthcare epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 44:159–177CrossRefPubMedGoogle Scholar
  27. Devriese L, Baele M, Butaye P (2006) The genus Enterococcus: taxonomy. PRO 4:163–174Google Scholar
  28. Drew RH (2009) Antimicrobial stewardship programs: how to start and steer a successful program. J Manag Care Pharm 15:S18–S23PubMedGoogle Scholar
  29. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolated. Appl Environ Microbiol 67(4):1628–1635CrossRefPubMedPubMedCentralGoogle Scholar
  30. EFSA (2012) Guidance for assessing the safety of Enterococcus faecium in animal feed. EFSA J 10:2682.  https://doi.org/10.2903/j.efsa.2012.2682CrossRefGoogle Scholar
  31. EFSA Panel on Biological Hazards (2011) Scientific opinion on risk-based control of biogenic amine formation in fermented foods. EFSA J 9:2393CrossRefGoogle Scholar
  32. EFSA Panel on Biological Hazards, Ricci A, Allende A, Bolton D, Chemaly M et al (2017) Scientific opinion on the update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA. EFSA J 15:e04664Google Scholar
  33. El-Din BB, El-Soda M, Ezzat N (2002) Proteolytic, lipolyticand autolytic activities of Enterococci strains isolated from Egyptian dairy products. Lait 82:289–304pCrossRefGoogle Scholar
  34. Erginkaya Z, Tatlı D, Yalanca I, Ünal E (2010) The determination of antibiotic resistance of Enterococcus spp. isolated from some traditional dairy and meat products (ECCO XXIX) annual meeting, Istanbul-TürkiyeGoogle Scholar
  35. Franz CMAP, Holzapfel WH, Stıles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1–24CrossRefPubMedGoogle Scholar
  36. Franz CMAP, Muscholl-Silberhorn AB, Yousıf NMK, Vancanneyt M, Swıngs J, Holzapfel WH (2001) The incidence of virulence factors and antibiotic resistance among Enterococci isolated from food. Appl Environ Microbiol 67(9):4385–4389CrossRefPubMedPubMedCentralGoogle Scholar
  37. Franz CM, Belkum MJV, Holzapfel WH, Abrıouel H, Galvez A (2007) Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol Rew 31:293–310CrossRefGoogle Scholar
  38. Franz CMAP, Huch M, Abrıouel H, Holzapfel W, Galvez A (2011) Enterococci as probiotics and their implications in food safety. Int J Food Microbiol Rev 151:128–140Google Scholar
  39. Freitas AR, Novaıs C, Ruız-Garbajosa P, Couque TM, Peıxe L (2009) Clonal expansion within clonal complex 2 and spread of vancomycin-resistant plasmids aamong different genetic lineages of Enterococcus faecalis from Portugal. J Antimicrobial Chemother 63:1104–1111CrossRefGoogle Scholar
  40. Gambrotto K, Ploy M, Dupron F, Giangiobbe M, Denis F (2001) Occurrence of vancomycin-resistant enterococci in pork and poultry products from a cattle-rearing area of France. J Clin Microbiol 39:2354–2355CrossRefGoogle Scholar
  41. Gelsomino R, Vancanneyt M, Codon S, Swıngs J, Cogan TM (2001) Enterococcal diversity in the environment of an Irish Cheddar-type cheesemaking factory. Int J Food Microbiol 71:177–188CrossRefPubMedGoogle Scholar
  42. Ghidan A, Dobay O, Kaszanyıtzky EJ, Samu P, Amyes SG, Nagy K, Rozgonyi F (2008) Vancomycin-resistant Enterococci (VRE) still persist in slaughtered poultry in Hungary 8 years after the ban on avoparcin. Acta Microbiol Immunol Hung 55(4):409–417CrossRefPubMedGoogle Scholar
  43. Giraffa G (2002) Enterococci from food. FEMS Microbiol Rev 26:163–171pCrossRefPubMedGoogle Scholar
  44. Giraffa G (2003) Functionality of Enterococci in dairy products. Int J Food Microbiol 88(2–3):215–222CrossRefPubMedGoogle Scholar
  45. Giraffa G, Sısto F (1997) Susceptibility to vancomycin of Enterococci isolated from dairy products. Lett Appl Microbiol 25:335–338sCrossRefPubMedGoogle Scholar
  46. Gomes BC, Esteves CT, Palazzo IC, Darini AL, Felis GE, Sechi LA, Franco B, De Martinis EC (2008) Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol 25(5):668–675CrossRefPubMedGoogle Scholar
  47. Guerrero-Ramos E, Molina-González D, Blanco-Morán S, Igrejas G, Poeta P, Alonso-Calleja C, Capita R (2016) Prevalence, antimicrobial resistance, and genotypic characterization of vancomycin-resistant enterococci in meat preparations. J Food Protect 79(5):748–756CrossRefGoogle Scholar
  48. Harbarth S, Cosgrove S, Carmeli Y (2002) Effects of antibiotics on nosocomial epidemiology of vancomycin-resistant enterococci. Antimicrob Agents Chemother 46:1619–1628CrossRefPubMedPubMedCentralGoogle Scholar
  49. Hasman H, Villadsen AG, Aarestrup FM (2005) Diversity and stability of plasmids from glycopeptides-resistant Enterococcus faecium (GRE) isolated from pigs in Denmark. Microb Drug Resist 11:178–184pCrossRefPubMedGoogle Scholar
  50. Hauben JH (2003) The potential of vancomycin-resistant enterococci to persist in fermented and pasteurised meat products. Int J Food Microbiol 88(1):11–18pCrossRefGoogle Scholar
  51. Hershberger E, Oprea SF, Donabedian SM, Perri M, Bozigar P, Bartlett P, Zervos MJ (2005) Epidemiology of antimicrobial resistance in enterococci of animal origin. J Antimicrobial Chemother 55(1):127–130CrossRefGoogle Scholar
  52. Hugas M, Garigga M, Aymerich MT (2003) Functionality of Enterococci in meat products. Int J Food Microbiol 88(2–3):233Google Scholar
  53. Hummel AS, Hertel C, Holzapfel WH, Franz CM (2007) Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl Environ Microbiol 73(3):730–739CrossRefPubMedGoogle Scholar
  54. Jensen LB, Ahrens P, Dons L, Jones RN, Hammerum A, Aarestrup FM (1998) Molecular analysis of the Tn1546 from vancomycin resistant enterococci isolated from animals and humans. J Clin Microbiol 36:437–42pPubMedPubMedCentralGoogle Scholar
  55. Joerger RD (2003) Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poult Sci 82:640–647CrossRefPubMedGoogle Scholar
  56. Karakaş A (2005) Isolation and identification of Enterococcus faecium from Beyaz cheese and fermented sucuks. Master of Science thesis of Institute of Science Cukurova University, Adana, TukeyGoogle Scholar
  57. Khodaee M, Nejad S (2017) Isolation and molecular identification of Enterococcus faecium strain C2 producing bacteriosins with wide antibacterial activity spectrum of local dairy products Zarand. J Innovat Food Sci Technol 9(4):Pe49–Pe58Google Scholar
  58. Klare I, Konstabel C, Badstubner D, Werner G, Witte W (2003) Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol 88:269–290pCrossRefPubMedGoogle Scholar
  59. Leavis HL, Bonten MJM, Williems RJL (2006) Identification of high-risk Enterococcal clonal complexes: global distribution and antibiotic resistance. Curr Opin Microbiol 9:454–460CrossRefPubMedGoogle Scholar
  60. Lee CR, Cho H III, Jeong BC, Lee SH (2013) Strategies to minimize antibiotic resistance. Int J Environ Res Public Health 10:4274–4305CrossRefPubMedPubMedCentralGoogle Scholar
  61. Linaje R, Coloma MD, Perez-Martınez G, Zunıga M (2004) Characterization of faecal Enterococci from rabits for the selection of probiotic strains. J Appl Microbiol 96:761–771CrossRefPubMedGoogle Scholar
  62. Linden PK (2007) Optimizing therapy for vancomycin-resistant enterococci (VRE). Semin Respir Crit Care Med 28:632–645CrossRefPubMedGoogle Scholar
  63. Lloyd DH (2012) Alternatives to conventional antimicrobial drugs: a review of future prospects. Vet Dermatol 23:299–304pCrossRefPubMedGoogle Scholar
  64. Lukasova J, Sustackova A (2003) Enterococci and antibiotic resistance. Acta Vet Brno 72:315–323CrossRefGoogle Scholar
  65. Mannu L, Paba A, Daga E, Comunian R, Zanetti S, Dupre I, Sechi LA (2003) Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcusfaecium strains of dairy, animal and clinical origin. Int J Food Microbiol 88(2–3):291–304CrossRefPubMedGoogle Scholar
  66. Marekova M, Laukova A, De Vuyst L, Nes IF (2003) Partial characterization of bacteriocins produced enviromental strain Enterococcus faecium EK13. J Appl Microbiol 94:523–530CrossRefPubMedGoogle Scholar
  67. Maschieto A, Martınez R, Palazzo ICV, Darını ALC (2004) Antimicrobial resistance of Enterococcus spp. isolated from the intestinal tract of patients from a University Hospital in Brazil. Mem Inst Oswaldo Cruz 99:763–767CrossRefPubMedGoogle Scholar
  68. Meier F, Lacroix C, Meile L, Jans C (2018) Enterococci and pseudomonads as quality indicators in industrial production and storage of mozzarella cheese from raw cow milk. Int Dairy J 82:28–34CrossRefGoogle Scholar
  69. Moehring RW, Anderson DJ (2012) Antimicrobial stewardship as part of the infection prevention effort. Curr Infect Dis Rep 14:592–600CrossRefPubMedGoogle Scholar
  70. Morrison D, Woodford N, Cookson B (1997) Enterococci as emerging pathogens of humans. J Appl Microbiol Suppl 83:89–99pCrossRefGoogle Scholar
  71. Murray BE (1998) Diversity among multidrug-resistant enterococci. Emerg Infect Dis 4:37–47CrossRefPubMedPubMedCentralGoogle Scholar
  72. Murrey BE (2000) Vancomycin resistant enterococcal infections. N Engl J Med 342:710–721CrossRefGoogle Scholar
  73. Novais C, Coque TM, Costa MJ, Sousa JC, Baquero F, Peixe LV (2005) High occurrence and persistence of antibiotic-resistant enterococci in poultry food samples in Portugal. J Antimicrob Chemother 56(6):1139–1143CrossRefPubMedGoogle Scholar
  74. Ogier J-C, Serror P (2008) Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol 126:291–301CrossRefPubMedGoogle Scholar
  75. Papamanoli E, Tzanestakis N, Litopoulou-Tzanetaki E, Kotzekidou P (2003) Characterization of lactic acid bacteria isolated from a Greek dry-Sausages in respect of their technological and probiotic properties. Meat Sci 65:859–867CrossRefPubMedGoogle Scholar
  76. Paterson DL (2006) The role of antimicrobial management programs in optimizing antibiotic prescribing within hospitals. Clin Infect Dis 42:S90–S95CrossRefPubMedGoogle Scholar
  77. Pearson H (2002) ‘Superbug’ hurdles key drug barrier. Nature 418:463CrossRefGoogle Scholar
  78. Potter A, Gerdts V, Littel-van den Hurk S (2008) Veterinary vaccines: alternatives to antibiotics? Anim Health Res Rev 9:187–199CrossRefPubMedGoogle Scholar
  79. Ribeiro T, Oliveira M, Fraqueza MJ, Laukova A, Elias M, Tenreiro R, Barretto AS, Semedo-Lemsaddek T (2011) Antibiotic resistance and virulence factors among enterococci isolated from Chouriço, a traditional portuguese dry fermented sausage. J Food Prot 74(3):465–469CrossRefPubMedGoogle Scholar
  80. Rinkinen M, Jalava K, Westermarck E, Salminen S, Ouwehand AC (2003) Interaction between probiotic lactic acid bacteria and canine enteric pathogens: a risk factor for intestinal Enterococcus faecium colonization. Veterin Microbiol 92:111–119CrossRefGoogle Scholar
  81. Rizzotti L, La Gioira F, Dellaglio F, Torriani S (2009) Molecular diversity and transferability of the tetracycline resistance gene tet(M), carried on Tn916-1545 family transposons, in enterococci from a total food chain. Antonie Van Leeuwenhoek 96(1):43–52pCrossRefPubMedGoogle Scholar
  82. Ross RP, Morgen S, Hill C (2002) Preservation and fermentation: past, present, and future. Int J Food Microbiol 79:3–16CrossRefPubMedGoogle Scholar
  83. Sabia C, De Niederhausern S, Guerrieri E, Messi P, Anacarso I, Manicardı G, Bondi M (2008) Detection of bacteriocin production and virülence traits in vancomycin-resistant enterococci of different sources. J Appl Microbiol 104(4):970–99pCrossRefPubMedGoogle Scholar
  84. Salem-Bekhit MM, Moussa MI, Muharram MM, Alanazy FK, Hefni HM (2012) Prevalence and antimicrobial resistance patern of multidrug-esistant enterococci isolated from clinical specimens. Int J Med Microbiol 30(1):44–51Google Scholar
  85. Samakupa AP (2003) Hygiene indicators in a fish processing establishment. University of Namibia, Department of Natural Resource, NamibiaGoogle Scholar
  86. Sanlibaba P, Senturk E (2018) Prevalence, characterization and antibiotic resistance of enterococci from traditional cheeses in Turkey. Int J Food Propert 21(1):1955–1963CrossRefGoogle Scholar
  87. Sarantinopoulos P, Kalantzopoulos G, Tsakalidou E (2002) Effect of Enterococcus faecium on microbiological, physicochemical and sensory characteristic of Greek Feta cheese. Int J Food Microbiol 76:93–105CrossRefPubMedGoogle Scholar
  88. Shankar N, Baghdayan AS, Gilmore MS (2002) Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746–750CrossRefPubMedGoogle Scholar
  89. Son R, Nimita F, Rusul G, Nasreddin E, Samuel L, Nishibuchi M (1999) Isolation and molecular characterization of vancomycin-resistant Enterococcus faecium in Malaysia. Lett Appl Microbiol 29:118–122CrossRefPubMedGoogle Scholar
  90. Strompfova V, Laukova A, Ouwehand AC (2004) Selection of Enterococci for potential canine probiotic additives. Vet Microbiol 100(1–2):107–114CrossRefPubMedGoogle Scholar
  91. Talebi M, Sadeghi J, Rahimi F, Pourshafie MR (2015) Isolation and biochemical fingerprinting of vancomycin-resistant Enterococcus faecium from meat, chicken and cheese. Jundishapur J Microbiol 8:e15815pGoogle Scholar
  92. Tansuphasiri U, Khaminthakul D, Pandii W (2006) Antibiotic resistance of Enterococci isolated from frozen foods and environmental water. Southeast Asian J Trop Med Public Health 37(1):162–170PubMedGoogle Scholar
  93. Templer SP, Rohner P, Baumgartner A (2008) Relation of Enterococcus faecalis and Enterococcus faecium isolates from foods and clinical specimens. J Food Prot 71(10):2100–2104CrossRefPubMedGoogle Scholar
  94. Tendolkar PM, Baghdayan AS, Shankar N (2003) Pathogenic enterococci: new developments in the 21st century. Cell Mol Life Sci 60:2622–2636CrossRefPubMedGoogle Scholar
  95. Tenover FC, Weigel LM, Appelbaum PC et al (2004) Vancomycin-resistant Staphylococcus aureus isolates from a patient in Pennsylvania. Antimicrob Agents Chemother 48:275–280CrossRefPubMedPubMedCentralGoogle Scholar
  96. Teuber M, Perreten V, Wirsching F (1996) Antibiotikumresistente Bakterien: Eine neue Dimension in der Lebensmittelmikrobiologie. Lebensm-Technol 29:182–199Google Scholar
  97. Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76:115–137CrossRefPubMedGoogle Scholar
  98. Upadhyaya PMG, Ravikumar KL, Umapathy BL (2009) Review of virulence factors of enterococcus: an emerging nosocomial pathogen. Ind J Med Microbiol 27:301–305CrossRefGoogle Scholar
  99. Valenzuela AS, Omar NB, Lopez RL, Abriouel H, Lopez RL, Velyovic K, Canamero MM, Topisirrovic MKL, Galvez A (2009) Virulance factors, antibiotic resistance and bacteriocins in enterococci from artisan foods of animal origin. Food Control 20(4):381–385CrossRefGoogle Scholar
  100. Vehreschild MJGT, Haverkamp M, Biehl LM, Lemmen S, Fätkenheuer G (2018) Vancomycin-resistant enterococci (VRE): a reason to isolate? Infection 47(1):1–5Google Scholar
  101. Wegener HC, Madsen M, Nıelsen N, Aarestrup FM (1997) Isolation of vancomycin-resistant Enterococcus faecium from food. Int J Food Microbiol 35:57–66CrossRefPubMedGoogle Scholar
  102. Wegener HC, Aarestrup FM, Jensen LB, Hammerum AM, Bager F (1999) Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg Infect Dis 5(3):329–335CrossRefPubMedPubMedCentralGoogle Scholar
  103. Weigel LM, Clewell DB, Gıll SR, Clark NC, Mcdougal LK, Flanagan SE, Kolonay JF, Shetty J, Kıllgore GE, Tenover FC (2003) Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302:1569–1571CrossRefPubMedGoogle Scholar
  104. Woodford N (1998) Glycopeptide-resistant enterococci: a decade of experience. J Med Microbiol 47:849–862CrossRefPubMedGoogle Scholar
  105. Yaman F, Esendal O (2004) Balıklarda probiyotik kullanımı. Orlab on-line Mikrobiyoloji Dergisi 2(6):1–18Google Scholar
  106. Yurdakul E, Ergınkaya Z, Unal E (2009) The isolation of gram positive coccoids from chicken meat and the tetermination of antibiotic resistance in gram positive coccoids. CESAR: Central European Symposium on Antimicrobial Resistance, Zadar/Hırvatistan, 47Google Scholar
  107. Zommiti M, Cambronel M, Maillot O, Barreau M, Sebei K, Feuilloley M, Ferchichi M, Connil N (2018) Evaluation of probiotic properties and safety of Enterococcus faecium isolated from Artisanal Tunisian Meat “Dried Ossban”. Front Microbiol 9:1685CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mevhibe Terkuran
    • 1
    Email author
  • Emel Ünal Turhan
    • 2
  • Zerrin Erginkaya
    • 3
  1. 1.Department of Gastronomy and Culinary Arts, Kadirli School of Applied SciencesOsmaniye Korkut Ata UniversityOsmaniyeTurkey
  2. 2.Department of Food Technology, Kadirli School of Applied SciencesOsmaniye Korkut Ata UniversityOsmaniyeTurkey
  3. 3.Department of Food Engineering, Faculty of AgricultureCukurova UniversityAdanaTurkey

Personalised recommendations