Microbial pathogen control in the beef chain: Recent research advances

Meat Science

Volumn 97, Issue 3, 2014, Pages 288-297

  Buncic, Sava ^a   Nychas, George John ^b   Lee, Michael R F ^c   Koutsoumanis, Kostas ^d   Hébraud, Michel ^e   Desvaux, Mickaël ^e   Chorianopoulos, Nikos ^b   Bolton, Declan ^f   Blagojevic, Bojan ^a   Antic, Dragan ^a  

^a Horticulture and Landscape Architecture   (Serbia)

^b AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^c ABERYSTWYTH UNIVERSITY   (United Kingdom)

^d ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^e CEMAGREF   (France)

^f TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

Beef chain; Beef safety; Control; Foodborne pathogens

Indexed keywords

CONTROL; FOOD SAFETY; MEATS; PATHOGENS; RESEARCH; RISK ASSESSMENT; SAFETY ENGINEERING;

FOOD-BORNE PATHOGENS; MICROBIAL PATHOGENS; MULTIPLE POINTS; RECENT RESEARCHES; RISK REDUCTIONS; TIME TEMPERATURE;

CHAINS;

BOS;

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL HUSBANDRY; BOVINE; ENTEROBACTERIACEAE; FOOD CONTROL; FOOD HANDLING; HUMAN; MEAT; MICROBIOLOGY; SANITATION; SLAUGHTERHOUSE;

ABATTOIRS; ANIMAL HUSBANDRY; ANIMALS; ANTI-INFECTIVE AGENTS; CATTLE; ENTEROBACTERIACEAE; FOOD HANDLING; FOOD MICROBIOLOGY; HUMANS; MEAT; SANITATION;

EID: 84899099586     PISSN: 03091740     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meatsci.2013.04.040     Document Type: Article

References (72)

1. Ammor M.S., Argyri A., Nychas G.-J.E. Rapid monitoring of the spoilage of minced beef stored under conventionally and active packaging conditions using Fourier transform infrared spectroscopy in tandem with chemometrics. Meat Science 2009, 81:507-514.
2. Antic D., Blagojevic B., Buncic S. Treatment of cattle hides with Shellac solution to reduce hide-to-beef microbial transfer. Meat Science 2011, 88:498-502.
3. Antic D., Blagojevic B., Ducic M., Mitrovic R., Nastasijevic I., Buncic S. Treatment of cattle hides with Shellac-in-ethanol solution to reduce bacterial transferability-A preliminary study. Meat Science 2010, 85:77-81.
4. Antic D., Blagojevic B., Ducic M., Nastasijevic I., Mitrovic R., Buncic S. Distribution of microflora on cattle hides and its transmission to meat via direct contact. Food Control 2010, 21:1025-1029.
5. Ashby K.D., Wen J., Chowdhury P., Casey T.A., Rasmussen M.A., Petrich J.W. Fluorescence of dietary porphyrins as a basis for real-time detection of fecal contamination on meat. Journal of Agricultural and Food Chemistry 2003, 51:3502-3507.
6. Bae W., Kaya K.N., Hancock D.D., Call D.R., Park Y.H., Besser T.E. Prevalence and antimicrobial resistance of thermophilic Campylobacter spp. from cattle farms in Washington State. Applied and Environmental Microbiology 2005, 71:169-174.
7. Birk T., Knøchel S. Fate of food-associated bacteria in pork as affected by marinade, temperature, and ultrasound. Journal of Food Protection 2009, 72:549-555.
8. Blagojevic B., Antic A., Adzic B., Tasic T., Ikonic P., Buncic S. Decontamination of beef raw material to improve safety of raw-fermented sausages. Proceeding of International Conference "Biological Food Safety and Quality", 4-5 October 2012, Belgrade, Serbia 2012, 81-83.
9. Blagojevic B., Antic D., Buncic S. A qualitative risk ranking of, and main control strategies for, biological hazards in relation to safety of chilled beef carcasses. Proceeding of International Conference "Biological Food Safety and Quality", 4-5 October 2012, Belgrade, Serbia 2012, 121-124.
10. Blagojevic B., Antic D., Ducic M., Buncic S. A study of Haptoglobin levels in groups of cattle and pigs with and without abnormalities at meat inspection. Foodborne Pathogens and Disease 2011, 8:1119-1124.
11. Blagojevic B., Antic D., Ducic M., Buncic S. Ratio between carcass- and skin microflora as an abattoir process hygiene indicator. Food Control 2011, 22:186-190.
12. Blagojevic B., Antic D., Ducic M., Buncic S. Visual cleanliness scores of cattle at slaughter and microbial loads on the hides and the carcases. Veterinary Record 2012, 170:563.
13. Bolton D.J., Doherty A.M., Sheridan J.J. Beef HACCP: Intervention and non-intervention systems. International Journal of Food Microbiology 2001, 66:119-129.
14. Bolton D.J., Monaghan A., Byrne B., Fanning S., Sweeney T., McDowell D.A. Incidence and survival of non-O157 verocytotoxigenic Escherichia coli in soil. Journal of Applied Microbiology 2011, 111:484-490.
15. Brichta-Harhay D.M., Arthur T.M., Bosilevac J.M., Kalchayanand N., Schmidt J.W., Wang R., Shackelford S.D., Loneragan G.H., Wheeler T.L. Microbiological analysis of bovine lymph nodes for the detection of Salmonella enterica. Journal of Food Protection 2012, 75:854-858.
16. Buncic S. Integrated food safety and veterinary public health 2006, CABI International Publishing, Wallingford, Oxfordshire, UK.
17. Burfoot D., Tinker D., Thorn R., Howell M. Use of fluorescence imaging as a hygiene indicator for beef and lamb carcasses in UK slaughterhouses. Biosystems Engineering 2011, 109:175-185.
18. Carpentier B., Cerf O. Persistence of Listeria monocytogenes in food industry equipment and premises. International Journal of Food Microbiology 2011, 145:1-8.
19. Carvalho C.M., Gannon B.W., Halfhide D.E., Santos S.B., Hayes C.M., Roe J.M., Azeredo J. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiology 2010, 10:232.
20. Casey, T. A., Rasmussen, M. A., & Petrich, J. W. (1999). Method and system for detecting fecal and ingesta contamination on the carcasses of meat animals. U.S. patent 5,914,247.
21. Coffey B., Rivas L., Duffy G., Coffey A., Ross R.P., McAuliffe O. Assessment of Escherichia coli O157:H7-specific bacteriophages e11/2 and e4/1c in model broth and hide environments. International Journal of Food Microbiology 2011, 147:188-194.
22. EFSA Scientific/technical report submitted to EFSA estimation of the relative contribution of different food and animal sources to human Salmonella infections in the European Union. Submitted by DTU Food in response to Question No. EFSA-Q-2010-00685 2011.
23. EFSA Scientific opinion on the public health hazards to be covered by inspection of meat (swine). EFSA Journal 2011, 2351.
24. EFSA Scientific opinion on the public health hazards to be covered by inspection of meat (poultry). EFSA Journal 2012, 2012b:2741.
25. EFSA The European Union summary report on trends and sources of zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 2012, 10(3):2597. (442 pp.).
26. Ennis C., McDowell D.A., Bolton D.J. The prevalence, distribution and characterisation of shiga toxin-producing Escherichia coli (STEC) serotypes and virulotypes from a cluster of bovine farms. Journal of Applied Microbiology 2012, 113:1238-1248.
27. FSA Red meat safety & clean livestock Available at:, (Accessed: 27.11.2012). http://www.food.gov.uk/multimedia/pdfs/publication/redmeatsafety.pdf.
28. Gialamas H., Zinoviadou K.G., Biliaderis C.G., Koutsoumanis K.P. Development of a novel bioactive packaging based on the incorporation of Lactobacillus sakei into sodium-caseinate films for controlling Listeria monocytogenes in foods. Food Research International 2010, 43:2402-2408.
29. Gill C.O., Landers C. Microbiological effects of carcass decontaminating treatments at four beef packing plants. Meat Science 2003, 65:1005-1011.
30. Grau F.H. Campylobacter jejuni and Campylobacter hyointestinalis in the intestinal tract and on the carcasses of calves and cattle. Journal of Food Protection 1988, 51:857-861.
31. Hancock D., Besser T., Lejeune J., Davis M., Rice D. The control of VTEC in the animal reservoir. International Journal of Food Microbiology 2001, 66:71-78.
32. Harvey R.B., Hume M.E., Droleskey R.E., Edrington T.S., Sheffield C.L., Callaway T.R., Ziprin R.L., Scott H.M., Anderson R.C., Nisbet D.J. Further characterization of campylobacter isolated from U.S. dairy cows. Foodbourne Pathogens and Disease 2005, 2:182-187.
33. Howlett B., Bolton D.J., O'Sullivan C. Development of pre-requisite programmes and HACCP principles for Irish beef slaughterhouses 2005, Teagasc-The National Food Centre.
34. Hugas M., Tsigarida E. Pros and cons of carcass decontamination: the role of the European Food Safety Authority. Meat Science 2008, 78:43-52.
35. Inglis G.D., Kalischuk L.D., Busz H.W. Chronic shedding of Campylobacter species in beef cattle. Journal of Applied Microbiology 2004, 97:410-420.
36. Jankuloski D., Prodanov M., Angelovski L., Ratkova M., Kostova S., Sekulovski P. Research for role of official veterinary inspector in cross contamination of offal and carcass at slaughterline with use of marker microorganisms. Macedonian Veterinary Review 2009, 32:45-53. (in Macedonian language, with Abstract in English).
37. Jullien C., Benezech T., Gentil C.L., Boulange-Petermann L., Dubois P.E., Tissier J.P., Traisnel M., Faille C. Physico-chemical and hygienic property modifications of stainless steel surfaces induced by conditioning with food and detergent. Biofouling 2008, 24:163-172.
38. Kargiotou C., Katsanidis E., Rhoades J., Kontominas M., Koutsoumanis K. Efficacies of soy sauce and wine base marinades for controlling spoilage of raw beef. Food Microbiology 2011, 28:158-163.
39. Kerry J.P., O'Grady M.N., Hogan S.A. Past, current and potential utilisation of active and intelligent packaging systems for meat and muscle-based products: A review. Meat Science 2006, 74:113-130.
40. Kierek-Pearson K., Karatan E. Biofilm development in bacteria. Advances in Applied Microbiology 2005, 57:79-111.
41. Kim M.S., Lefcourt A.M., Chen Y.-R. Optimal fluorescence excitation and emission bands for detection of fecal contamination. Journal of Food Protection 2003, 66:1198-1207.
42. Koutsoumanis K., Tassou C.C., Nychas G.-J.E. Chapter 17 biogenic amines. Pathogens and toxins in foods: Challenges and interventions 2008, ASM Press, Washington, USA. V.K. Juneja, J.N. Sofos (Eds.).
43. Koutsoumanis K., Vaikousi C., Biliaderis C. Time temperature indicators can be used as an effective risk management tool for L. monocytogenes in ready-to-eat foods. International Symposium on Problems of Listeriosis ISOPOL XVII, Porto May 5-8, 2010, Portugal 2010, 52.
44. Kristo E., Koutsoumanis K.P., Biliaderis C.G. Thermal, mechanical and water vapor barrier properties of sodium caseinate films containing antimicrobials and their inhibitory action on Listeria monocytogenes. Food Hydrocolloids 2008, 22:373-386.
45. Lee M.R.F., Scott M.B., Veberg Dahl A., Evans P.R., Theobald V.J., Lundby F., Scollan N.D., Wold J.-P. Potential of chlorophyll-rich feed ingredients to improve detection of fecal contamination in the abattoir. Journal of Food Protection 2013, 76:516-522.
46. Lee M.R.F., Theobald V.J., Ougham H.J., Veberg Dahl A., Lundby F., Scollan N.D., Wold J.-P. Natural fecal fluorophores and the potential of chlorophyll based markers to optimise fluorescence as a real-time solution for the detection of fecal contamination on carcasses. Meat Science 2010, 86:966-975.
47. Lefcourt A.M., Kim M.S., Chen Y.-R. A transportable fluorescence imaging system for detecting fecal contaminants. Computers and Electronics in Agriculture 2005, 48:63-74.
48. Loretz M., Stephan R., Zweifel C. Antibacterial activity of decontamination treatments for cattle hides and beef carcasses. Food Control 2011, 22:347-359.
49. Maunsell B., Bolton D.J. Guidelines for food safety management on farms 2004, Teagasc-The National Food Centre.
50. Murata H., Shimada N., Yoshioka M. Current research on acute phase proteins in veterinary diagnosis: an overview. Veterinary Journal 2004, 168:28-40.
51. Nørrung B., Andersen J.K., Buncic S. Main concerns of pathogenic microorganisms in meat. Safety of meat and processed meat 2009, 3-29. Springer, New York. F. Todra (Ed.).
52. Nørrung B., Buncic S. Microbial safety of meat in the European Union. Meat Science 2008, 78:14-24.
53. Northen J.R. Using farm assurance schemes to signal food safety to multiple food retailers in the UK. International Food and Agribusiness Management Review 2001, 4:37-50.
54. Nychas G.-J.E., Skandamis P., Tassou C.C., Koutsoumanis K. Meat spoilage during distribution. Meat Science 2008, 78:77-89.
55. O'Neill C.J., Bolton D.J., Fanning S. Comparative studies on the survival of verocytotoxigenic Escherichia coli and Salmonella in different farm environments. Agriculture, Food and Analytical Bacteriology 2011, 1:116-122.
56. Quinon E., Chamot S., Groelly J., Chavant P., Bernardi T., Desvaux M., Christieans S., Hebraud M. Tests d'efficacité de l'action curative et préventive de produits de décontamination sur des biofilms de Listeria monocytogenes. Viandes et Produits Carnés, Hors Série 2010, 181-182.
57. Reid C.-A., Small A., Avery S.M., Buncic S. Presence of foodborne pathogens on cattle hides. Food Control 2002, 13:411-415.
58. Renier S., Hebraud M., Desvaux M. Molecular biology of surface colonization by Listeria monocytogenes: An additional facet of a Gram-positive foodborne pathogen. Environmental Microbiology 2011, 13:835-850.
59. Rhoades J.R., Duffy G., Koutsoumanis K. Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: A review. Food Microbiology 2009, 26:357-376.
60. Roberts T.A. Contamination of meat: The effects of slaughter practices on the bacteriology of the red meat carcass. Royal Society of Health Journal 1980, 100:3-9.
61. Saá P., Cabo M.L., Rodríguez J.J. Effects of mussel processing soils on the adherence of Listeria monocytogenes to polypropylene and stainless steel. Journal of Food Protection 2009, 72:1885-1890.
62. Sagatarame S., Theobald V.J., Fleming H.R., Leemans D., Gay A., Lee M.R.F. Effectiveness of supplementing drinking water with Magnesium Chlorophyllin to increase fecal fluorescence in sheep, as an aid to increase detection of contamination in the abattoir. Proceeding of International Conference "Biological Food Safety and Quality", 4-5 October 2012, Belgrade, Serbia 2012, 75-77.
63. Skandamis P.N., Nychas G.-J.E. Preservation of fresh meat with active and modified atmosphere packaging conditions. International Journal of Food Microbiology 2002, 79:35-45.
64. Sofos J. The food chain approach to food safety and quality. Proceeding of International Conference "Biological Food Safety and Quality", 4-5 October 2012, Belgrade, Serbia 2012, 1-4.
65. Stopforth J.D., Sofos J.N. Recent advances in pre- and post-slaughter intervention strategies for control of meat contamination. Advances in microbial food safety, ACS Symposium 931. Recent advances in intervention strategies to improve food safety 2006, 66-86. Amer. Chem. Soc., Oxford Univ. Press, Washington, D.C., USA. V.J. Juneja, J.P. Cherry, M.H. Tunick (Eds.).
66. Tergney A., Bolton D.J. Validation studies on an online monitoring system for reducing faecal and microbial contamination on beef carcasses. Food Control 2006, 17:378-382.
67. Vaikousi H., Biliaderis C.G., Koutsoumanis K.P. Development of a microbial time/temperature indicator prototype for monitoring the microbiological quality of chilled foods. Applied and Environmental Microbiology 2008, 74:3242-3250.
68. Vaikousi H., Biliaderis C.G., Koutsoumanis K.P. Applicability of a microbial Time Temperature Indicator (TTI) for monitoring spoilage of modified atmosphere packed minced meat. International Journal of Food Microbiology 2009, 133:272-278.
69. Veberg A., Sorheim O., Moan J., Iani V., Juzenas P., Nilsen A.N., Wold J.P. Measurement of lipid oxidation and porphyrins in high oxygen modified atmosphere and vacuum-packed minced turkey and pork meat by fluorescence spectra and images. Meat Science 2006, 73:511-520.
70. Wagenaar J.A., Van Bergen M., Mueller M.A., Wassenaar T.M., Carlton R.M. Phage therapy reduces Campyobacter jejuni colonization in broilers. Veterinary Microbiology 2005, 109:275-283.
71. Whitehead K.A., Smith L.A., Verran J. The detection and influence of food soils on microorganisms on stainless steel using scanning electron microscopy and epifluorescence microscopy. International Journal of Food Microbiology 2010, 141:S125-S133. (Supplement).
72. Zinoviadou K.G., Koutsoumanis K.P., Biliaderis C.G. Physical and thermo-mechanical properties of whey protein isolate films containing antimicrobials, and their effect against spoilage flora of fresh beef. Food Hydrocolloids 2010, 24:49-59.