Phage inactivation of Staphylococcus aureus in fresh and hard-type cheeses

International Journal of Food Microbiology

Volumn 158, Issue 1, 2012, Pages 23-27

  Bueno, Edita ^a   García, Pilar ^a   Martínez, Beatriz ^a   Rodríguez, Ana ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

Biocontrol; Cheese; Lytic phage; Staphylococcus aureus

Indexed keywords

ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOLYSIS; BACTERIOPHAGE; BACTERIUM ISOLATE; CHEESE; CHEESEMAKING; COLONY FORMING UNIT; CONTROLLED STUDY; CRYOPRESERVATION; FOOD CONTAMINATION; FOOD PROCESSING; LIMIT OF DETECTION; MICROORGANISM; MILK; NONHUMAN; PASTEURIZATION; PHYSICAL CHEMISTRY; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIOPHAGES; CHEESE; FOOD CONTAMINATION; MILK; PASTEURIZATION; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 84864383139     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.06.012     Document Type: Article

References (48)

1. Alomar J., Lebert A., Montel M.C. Effect of temperature and pH on growth of Staphylococcus aureus in co-culture with Lactococcus garvieae. Current Microbiology 2008, 56:408-412.
2. Atterbury R.J., Connerton P.L., Dodd C.E., Rees C.E., Connerton I.F. Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Applied and Environmental Microbiology 2003, 69:6302-6306.
3. Belay N., Rasooly A. Staphylococcus aureus growth and enterotoxin A production in an anaerobic environment. Journal of Food Protection 2002, 65:199-204.
4. Bigwood T., Hudson J.A., Billington C. Influence of host and bacteriophage concentration on the inactivation of food-borne pathogenic bacteria by two phages. FEMS Microbiology Letters 2009, 291:59-64.
5. Brüssow H., Canchaya C., Hardt W.D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiology and Molecular Biology Reviews 2004, 68:560-602.
6. Bruttin A., Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrobial Agents and Chemotherapy 2005, 49:2874-2878.
7. Cairns B.J., Timms A.R., Jansen V.A.A., Connerton I.F., Payne R.J.H. Quantitative models of in vitro bacteriophage-host dynamics and their application to phage therapy. PLoS Pathogens 2009, 5:1-10.
8. Cárcoba R., Delgado T., Rodríguez A. Comparative performance of a mixed strain starter in cow's milk, ewe's milk and mixtures of these milks. European Food Research and Technology 2000, 211:141-146.
9. Carlton R.M., Noordman W.H., Biswas B., de Meester E.D., Loessner M.J. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regulatory Toxicology and Pharmacology 2005, 43:301-312.
10. Cheng J., Novick R.P. Phage-mediated intergeneric transfer of toxin genes. Science 2009, 323:139-141.
11. Commission regulation (EC) no. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs, European Commission, Brussels, Belgium.
12. De Buyser M.L., Dufour B., Maire M., Lafarge V. Implication of milk and milk products in foodborne diseases in France and in different industrialised countries. International Journal of Food Microbiology 2001, 67:1-17.
13. Deasy T., Mahony J., Neve H., Heller K.J., van Sinderen D. Isolation of a virulent Lactobacillus brevis phage and its application in the control of beer spoilage 2011.
14. Delbes C., Alomar J., Chougui N., Martin J., Montel M.C. Staphylococcus aureus growth and enterotoxin production during manufacture of non-cooked, semi-hard cheese from cow's raw milk. Journal of Food Protection 2006, 69:2161-2167.
15. Dinges M.M., Orwin P.M., Schlievert P.M. Exotoxins of Staphylococcus aureus. Clinical Microbiology Reviews 2000, 13:16-34.
16. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal 2011, 9(2090):1-378.
17. Gálvez A., Abriouel H., Benomar N., Lucas R. Microbial antagonists to food-borne pathogens and biocontrol. Current Opinion in Biotechnology 2010, 21:142-148.
18. García P., Madera C., Martínez B., Rodríguez A. Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. International Dairy Journal 2007, 17:1232-1239.
19. García P., Martínez B., Obeso J., Rodríguez A. Bacteriophages and their applications in food safety. Letters in Applied Microbiology 2008, 47:479-485.
20. García P., Madera C., Martínez B., Rodríguez A., Suárez J.E. Prevalence of bacteriophages infecting Staphylococcus aureus in dairy samples and their potential as biocontrol agents. Journal of Dairy Science 2009, 92:3019-3026.
21. García P., Rodríguez L., Rodríguez A., Martínez B. Food biopreservation: promising strategies using bacteriocins, bacteriophages and endolysins. Trends in Food Science and Technology 2010, 21:373-382.
22. Gill J.J., Sabour P.M., Leslie K.E., Griffiths M.W. Bovine whey proteins inhibit the interaction of Staphylococcus aureus and bacteriophage K. Journal of Applied Microbiology 2006, 101:377-386.
23. Guenther S., Loessner M.J. Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 2011, 1:94-100.
24. Guenther S., Huwyler D., Richard S., Loessner M.J. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Applied and Environmental Microbiology 2009, 75:93-100.
25. Hagens S., Offerhaus M.L. Bacteriophages - new weapons for food safety. Food Technology 2008, 62:46-54.
26. IDF Standard 152 Milk and milk products. Determination of fat content. General guidance on the use of butyrometric methods 1991, International Dairy Federation, Brussels, Belgium.
27. IDF Standard 20B Milk. Determination of nitrogen content. Part 1: Kjeldahl method 1993, International Dairy Federation, Brussels, Belgium.
28. IDF Standard 4A Cheese and processed cheese. Determination of the total solids content (reference method) 1982, International Dairy Federation, Brussels, Belgium.
29. Ito A., Sato Y., Kudo S., Sato S., Nakajima H., Toba T. The screening of hydrogen peroxide-producing lactic acid bacteria and their application to inactivating psychrotrophic food-borne pathogens. Current Microbiology 2003, 47:231-236.
30. Katsuda K., Hata E., Kobayashi H., Kohmoto M., Kawashima K., Tsunemitsu H., Eguchi M. Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Veterinary Microbiology 2005, 105:301-305.
31. Kim K.P., Klumpp J., Loessner M.J. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. International Journal of Food Microbiology 2007, 115:195-203.
32. Lanciotti R., Sinigaglia M., Gardini F., Vannini L., Guerzoni M.E. Growth/no growth interfaces of Bacillus cereus, Staphylococcus aureus and Salmonella enteritidis in model systems based on water activity, pH, temperature and ethanol concentration. Food Microbiology 2001, 18:659-668.
33. Le Loir Y., Baron F., Gautier M. Staphylococcus aureus and food poisoning. Genetics and Molecular Research 2003, 2:63-76.
34. Leverentz B., Conway W.S., Alavidze Z., Janisiewicz W.J., Fuchs Y., Camp M.J., Chighladze E., Sulakvelidze A. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. Journal of Food Protection 2001, 64:1116-1121.
35. Leverentz B., Conway W.S., Camp M.J., Janisiewicz W.J., Abuladze T., Yang M., Saftner R., Sulakvelidze A. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Applied and Environmental Microbiology 2003, 69:4519-4526.
36. Lindqvist R., Sylven S., Vagsholm I. Quantitative microbial risk assessment exemplified by Staphylococcus aureus in unripened cheese made from raw milk. International Journal of Food Microbiology 2002, 78:155-170.
37. Little C.L., Rhoades J.R., Sagoo S.K., Harris J., Greenwood M., Mithani V., Grant K., McLauchlin J. Microbiological quality of retail cheeses made from raw, thermized or pasteurized milk in the UK. Food Microbiology 2008, 25:304-312.
38. López-Pedemonte T., Brinez W.J., Roig-Sagues A.X., Guamis B. Fate of Staphylococcus aureus in cheese treated by ultrahigh pressure homogenization and high hydrostatic pressure. Journal of Dairy Science 2006, 89:4536-4544.
39. Mahony J., McAuliffe O., Ross R.P., van Sinderen D. Bacteriophages as biocontrol agents of food pathogens. Current Opinion in Biotechnology 2011, 22:157-163.
40. Meyrand A., Rozand C.V., Gonthier A., Mazuy C., Gueniot S.R., Jaubert G., Perrin, Lapeyre C., Richard Y. Main differences in behavior and enterotoxin production of Staphylococcus aureus in two different raw milk cheeses. Revue de Medécine Vétérinaire 1999, 150:271-278.
41. Modi R., Hirvi Y., Hill A., Griffiths M.W. Effect of phage on survival of Salmonella enteritidis during manufacture and storage of Cheddar cheese made from raw and pasteurized milk. Journal of Food Protection 2001, 64:927-933.
42. Obeso J.M., García P., Martínez B., Arroyo-López F.N., Garrido-Fernández A., Rodríguez A. Use of logistic regression for predicting Staphylococcus aureus fate in pasteurized milk in the presence of two lytic phages. Applied and Environmental Microbiology 2010, 76:6038-6046.
43. Rilla N., Martínez B., Rodríguez A. Inhibition of a methicillin-resistant Staphylococcus aureus strain in AfuegaD́l Pitu cheese by the nisin Z producing strain Lactococcus lactis subsp. lactis IPLA 729. Journal of Food Protection 2004, 67:928-933.
44. Sambrook J., Maniatis T., Fritsch E.F. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. second edition.
45. Schulz-Collins D., Senge B. Acid and acid/rennet-curd cheeses. Part A: quark, cream cheese and related varieties. Major Cheese Groups 2004, vol. 2:301-328. Elsevier Academic Press, San Diego, California. third edition. P.F. Fox, P.H. McSweeney, T.M. Cogan, T. Guinee (Eds.).
46. Tirado C., Schmidt K. WHO Surveillance Programme for Control of Foodborne Infections and Intoxications in Europe Seventh Report. http://www.bfr.bund.de/internet/7threport/7threp_fr.htm.
47. Waldvogel F.A. Staphylococcus aureus (including Staphylococcal toxic shock). Principles and Practice of Infectious Diseases 2001, 2069-2092. Churchill Livingstone, Philadelphia. J.L. Mandell, J.E. Bennet, R. Dolin (Eds.).
48. Whichard J.M., Sriranganathan N., Pierson F.W. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophages Felix O1 in liquid culture and on chicken frankfurters. Journal of Food Protection 2003, 66:220-225.