Antimicrobial susceptibility of bifidobacteria from probiotic milk products and determination of the genetic basis of tetracycline resistance in Enterococcus species after in vitro conjugation with Bifidobacterium animalis subsp. lactis

Food Control

Volumn 94, Issue , 2018, Pages 205-211

  Naghizadeh Raeisi, Shahram ^a,b   Ghoddusi, Hamid B ^a   Juncker Boll, Erik ^c   Farahmand, Nasim ^a   Stuer Lauridsen, Birgitte ^c   Johansen, Eric ^c   Sutherland, Jane P ^a   Ouoba, Labia Irène I ^a,d  

^a LONDON METROPOLITAN UNIVERSITY   (United Kingdom)

^b Islamic Azad University   (United Kingdom)

^c CHR HANSEN A S   (Denmark)

^d Ouoba Consulting   (United Kingdom)

Author keywords

Antimicrobial resistance; Bifidobacteria; Fermented milk products; Gene transfer; Genetic mutations; Probiotics

Indexed keywords

EID: 85053201679     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2018.07.016     Document Type: Article

References (46)

1. Aires, J., Doucet-Populaire, F., Butel, M., Tetracycline resistance mediated by tet(W), tet(M), and tet(O) genes of Bifidobacterium isolates from humans. Applied and Environmental Mirobiology 73 (2007), 2751–2754.
2. Ammor, M., Florez, A., Mayo, B., Antimicrobial resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiology 24 (2007), 559–570.
3. Barberis, C.M., Cittadini, R.M., Almuzara, M.N., Feinsilberg, A., Famiglietti, A.M., Ramírez, M.S., et al. Recurrent urinary infection with Bifidobacterium scardovii. Journal of Clinical Microbiology 50 (2012), 1086–1088.
4. Brodersen, D.E., Clemons, W.M. Jr., Carter, A.P., Morgan-Warren, R.J., Wimberly, B.T., Ramakrishnan, V., The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B, on the 30S ribosomal subunit. Cell 103 (2000), 1143–1154.
5. Charteris, W., Kelly, P., Morelli, L., Collins, J., Antimicrobial susceptibility of potentially probiotic Bifidobacterium isolates from the human gastrointestinal tract. Letters in Applied Microbiology 26 (1998), 333–337.
6. Cheikhyoussef, A., Pogori, N., Chen, W., Zhang, H., Antimicrobial proteinaceous compound obtained from bifidobacteria: From production to their application. International Journal of Food Microbiology 125 (2008), 215–222.
7. Connell, S.R., Trcaz, D.M., Nierhaus, K.H., Carter, A.P., Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrobial Agents and Chemotherapy 47 (2000), 3675–3681.
8. D'Souza, A., Rajkumar, C., Cooke, J., Bulpitt, J., Probiotics in prevention of antimicrobial associated diarrhoea: meta-analysis. British Medical Journal 324 (2002), 1361–1366.
9. EFSA BIOHAZ, Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2012 update). EFSA Journal, 10, 2012, 3020.
10. EFSA-BIOHAZ, Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed. EFSA Journal 923 (2008), 1–48.
11. EFSA-FEEDAP, Update of the criteria used in the assessment of bacterial resistance to antibiotics of human or veterinary importance. EFSA Journal 732 (2008), 1–15.
12. EFSA-FEEDAP, Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA Journal, 10(6), 2012, 2740.
13. EUROPA-CEU, Regulation 258/97/EC of the European parliament and of the council concerning novel foods and novel food ingredients. Official Journal of the European Union L43 (1997), 1–6.
14. EUROPA-CEU, Regulation (EC) N 178/2002 of the European parliament and of the council 28 January 2002, laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Official Journal of the European Union L31 (2002), 1–24.
15. EUROPA-CEU, Regulation 1831/2003/EC of the European parliament and of the council on additives for use in animal nutrition. Official Journal of the European Union L268 (2003), 29–43.
16. EUROPA-CEU, Regulation 1829/2003/EC of the European parliament and of the council on genetically modified food and feed. Official Journal of the European Union L268 (2003), 1–23.
17. FAO/WHO, Guidelines for the evaluation of probiotics in food: Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Joint FAO/WHO Working Group Report, 2002, 1–11.
18. Gueimonde, M., Florez, A., Hoek, A., Lauridsen, B., Stroman, P., Reyes-Gavilan, C., et al. Genetic basis of tetracycline resistance in Bifidobacterium animalis ssp. lactis. Applied and Environmental Microbiology 76 (2010), 3364–3369.
19. Gueimonde, M., Sánchez, B., de los Reyes-Gavilán, C.G., Margolles, A., Antimicrobial resistance in probiotic bacteria. Frontiers in Microbiology 4 (2013), 1–6.
20. van Hoek, A.H.A.M., Margolles, A., Damig, K.J., Korhonen, J.M., ZyckaKrzesinka, J., Bardowsky, J., et al. Molecular assessment of erythromycin and tetracycline resistance genes in lactic acid bacteria and bifidobacteria and their relation to the phenotypic resistance. International Journal of Probiotics and Prebiotics 3 (2008), 271–280.
21. Jenke, A., Ruf, E.M., Hoppe, T., Heldmann, M., Wirth, S., Bifidobacterium septicaemia in an extremely low-birthweight infant under probiotic therapy. Archives of Disease in Childhood - Fetal and Neonatal Edition 97 (2012), F217–F218.
22. Karlowsky, J., Jones, E., Importance of using current NCCLS breakpoints to interpret cefotaxime and ceftriaxone MICs for Streptococcus pneumonia. Journal of Antimicrobial Chemotherapy 51 (2003), 467–468.
23. Kastner, S., Perreten, V., Bleuler, H., Hugenschmidt, G., Lacroix, C., Meile, L., Antimicrobial susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. Systematic & Applied Microbiology 29 (2005), 145–155.
24. Kazimierczak, K.A., Flint, H.J., Scott, K.P., Comparative analysis of sequences flanking tet(W) resistance genes in multiple species of gut bacteria. Antimicrobial Agents and Chemotherapy 50 (2006), 2632–2639.
25. Kheadr, E., Bernoussia, N., Lacroixc, C., Fliss, I., Comparison of the sensitivity of commercial strains and infant isolates of bifidobacteria to antimicrobials and bacteriocins. International Dairy Journal 14 (2004), 1041–1053.
26. King, A., Phillips, I., The in vitro activity of daptomycin against 514 Gram positive aerobic clinical isolates. Journal of Antimicrobial Chemotherapy 48 (2001), 219–223.
27. Lahtinen, S.J., Boyle, R.J., Margolles, A., Frías, R., Gueimonde, M., Safety assessment of probiotics. Charalampopoulos, D., Rastall, R.A., (eds.) Prebiotics and probiotics science and technology, 2009, Springer-Verlag, Berlin, 1193–1225.
28. Laulund, S., Wind, A., Derkx, P.M.F., Zuliani, V., Regulatory and safety requirements for food cultures. Microorganisms, 5, 2017 E28.
29. Licht, T., Wilcks, A., Conjugative gene transfer in the gastrointestinal environment. Advances in Applied Microbiology 58 (2005), 77–95.
30. Lim, K., Huh, C., Baek, Y., Antimicrobial susceptibility of bifidobacteria. Journal of Dairy Science 76 (1993), 2168–2174.
31. Loquasto, J.R., Barrangou, R., Dudley, E.G., Stahl, B., Chen, C., Roberts, R.F., Bifidobacterium animalis subsp. lactis ATCC 27673 is a genomically unique strain within its conserved subspecies. Applied and Environmental Microbiology 79 (2013), 6903–6910.
32. Lupien, A., Gingras, H., Bergeron, M.G., Leprohon, P., Ouellette, M., Multiple mutations and increased RNA expression in tetracycline-resistant Streptococcus pneumoniae as determined by genome-wide DNA and mRNA sequencing. Journal of Antimicrobial Chemotherapy 70 (2014), 1946–1959.
33. Masco, L., Van Hoorde, K., De Brandt, E., Swings, J., Huys, G., Antimicrobial susceptibility of Bifidobacterium strains from humans, animals and probiotic products. Journal of Antimicrobial Chemotherapy 58 (2006), 85–94.
34. Mayrhofer, S., Mair, C., Kneifel, W., Domig, K.J., Susceptibility of bifidobacteria of animal origin to selected antimicrobial agents. Chemotherapy Research and Practice, 2011, 2011, 989520.
35. Moubareck, C., Gavini, F., Vaugien, L., Butel, M., Doucet-Populaire, F., Antimicrobial susceptibility of bifidobacteria. Journal of Antimicrobial Chemotherapy 55 (2005), 38–44.
36. Naghizadeh Raeisi, S., Ouoba, L.I.I., Farahmand, N., Sutherland, J., Ghoddusi, H.B., Variation, viability and validity of bifidobacteia in fermented milk products. Food Control 34 (2013), 691–697.
37. Nord, C., Sillerstrom, E., Wahlund, E., Effect of tigecycline on normal oropharyngeal and intestinal microflora. Antimicrobial Agents and Chemotherapy 50 (2006), 3375–3380.
38. Ohishi, A., Takahashi, S., Ito, Y., Ohishi, Y., Tsukamoto, K., Nanba, Y., et al. Bifidobacterium septicemia associated with postoperative probiotic therapy in a neonate with omphalocele. The Journal of Pediatrics 156 (2010), 679–681.
39. Ouoba, L.I.I., Lei, V., Jensen, L., Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: Determination and transferability of the resistance genes to other bacteria. International Journal of Food Microbiology 121 (2008), 217–224.
40. Ouoba, L.I.I., Parkouda, C., Diawara, B., Scotti, C., Varnam, A., Identification of Bacillus spp. from bikalga, fermented seeds of Hibiscus sabdariffa: Phenotypic and genotypic characterization. Journal of Applied Microbiology 104 (2008), 122–131.
41. Reuter, G., Klein, G., Goldberg, M., Identification of probiotic cultures in food samples. Food Research International 35 (2002), 117–124.
42. Russell, D., Ross, R., Fitzgerald, G., Stanton, C., Metabolic activities and probiotic potential of bifidobacteria. International Journal of Food Microbiology 149 (2011), 88–105.
43. Ruzauskas, M., Suziedeliene, E., Siugzdiniene, R., Seputiene, V., Povilonis, J., Antimicrobial resistance of Enterococcus spp. spread in poultry products in Lithuania. Journal of Food Safety 30 (2010), 902–915.
44. Thapar, N., Sanderson, R., Diarrhoea in children: An interface between developing and developed countries. The Lancet 363 (2004), 641–653.
45. Wang, N., Hang, X., Zhang, M., Liu, X., Yang, H., Analysis of newly detected tetracycline resistance genes and their flanking sequences in human intestinal bifidobacteria. Scientific Reports, 7, 2017, 6267.
46. Zhou, J., Pillidge, C., Gopal, P., Gill, H., Antimicrobial susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. International Journal of Food Microbiology 98 (2005), 211–217.