The efficacy of interventions applied during primary processing on contamination of beef carcasses with Escherichia coli: A systematic review-meta-analysis of the published research

Food Control

Volumn 27, Issue 2, 2012, Pages 385-397

  Greig, J D ^a   Waddell, L ^a,b   Wilhelm, B ^a,b   Wilkins, W ^c   Bucher, O ^a,b   Parker, S ^d   Rajic A ^a,b,d  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c Saskatchewan Ministry of Agriculture   (Canada)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Beef; Escherichia coli; Meta analysis; Pasteurization; Processing interventions; Systematic review

Indexed keywords

ESCHERICHIA COLI;

EID: 84861028239     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2012.03.019     Document Type: Review

References (82)

1. Algino R.J., Ingham S.C., Zhu J. Survey of antimicrobial effects of beef carcass intervention treatments in very small state-inspected slaughter plants. Journal of Food Science 2007, 72(5):M173-M179.
2. Bacon R.T., Belk K.E., Sofos J.N., Clayton R.P., Reagan J.O., Smith G.C. Microbial populations on animal hides and beef carcasses at different stages of slaughter in plants employing multiple-sequential interventions for decontamination. Journal of Food Protection 2000, 63(8):1080-1086.
3. Bacon R.T., Sofos J.N., Belk K.E., Smith G.C. A comparison of the three commercial beef carcass decontamination systems. Animal science research report 2000 2000, (pp. 45-51), Department of Animal Science Colorado State University, Fort Collins, CO.
4. Barkocy-Gallagher G.A., Arthur T.M., Rivera-Betancourt M., Nou X., Shackelford S.D., Wheeler T.L., et al. Seasonal prevalence of Shiga toxin-producing Escherichia coli, including O157:H7 and non-O157 serotypes, and Salmonella in commercial beef cattle processing plants. Journal of Food Protection 2003, 66(11):1978-1986.
5. Begg C.B., Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994, 50:1088-1101.
6. Belk K.E. Beef decontamination technologies 2001, Available at, Date last accessed 24.02.11. http://www.beefresearch.org/CMDocs/BeefResearch/ACFFC.pdf.
7. Benito Y., Pin C., Marin M.L., Garcia M.L., Selgas M.D., Casas C. Cell surface hydrophobicity and attachment of pathogenic and spoilage bacteria to meat surfaces. Meat Science 1997, 45:419-425.
8. Bland J.M., Altman D.G. Transforming data. BMJ 1996, 312:770.
9. Borenstein M., Hedges L.V., Higgins J.P.T., Rothstein H.R. Introduction to meta-analysis 2009, (pp. 21, 72, 107-125, 277-292), John Wiley & Sons, Chichester; Hoboken.
10. Bosilevac J.M., Nou X., Barkocy-Gallagher G.A., Arthur T.M., Koohmaraie M. Treatments using hot water instead of lactic acid reduce levels of aerobic bacteria and Enterobacteriaceae and reduce the prevalence of Escherichia coli O157:H7 on preevisceration beef carcasses. Journal of Food Protection 2006, 69(8):1808-1813.
11. Bosilevac J.M., Nou X., Osborn M.S., Allen D.M., Koohmaraie M. Development and evaluation of an on-line hide decontamination procedure for use in a commercial beef processing plant. Journal of Food Protection 2005, 68(2):265-272.
12. Bucher O. Evaluation of interventions for Salmonella in chickens using research synthesis and quantitative exposure assessment 2011, Available at, Accessed 12.09.11. http://gateway.proquest.com/openurl%3furl_ver=Z39.88-2004%26res_dat=xri:pqdiss%26rft_val_fmt=info:ofi/fmt:kev:mtx:dissertation%26rft_dat=xri:pqdiss:MR71460.
13. Bucher O., Fazil A., Rajić A., Farrar A., Wills R., McEwen S.A. Evaluating interventions against Salmonella in broiler chickens: applying synthesis research in support of quantitative exposure assessment. Epidemiology and Infection 2011, published online July 25. 10.1017/S0950268811001373.
14. Canadian Food Inspection Agency Food safety enhancement program manual 2011, Available at, Date last accessed 13.07.11. http://www.inspection.gc.ca/english/fssa/polstrat/haccp/manue/tablee.shtml.
15. Castillo A., Lucia L.M., Goodson K.J., Savell J.W., Acuff G.R. Comparison of water wash, trimming, and combined hot water and lactic acid treatments for reducing bacteria of fecal origin on beef carcasses. Journal of Food Protection 1998, 61(7):823-828.
16. Castillo A., Lucia L.M., Roberson D.B., Stevenson T.H., Mercado I., Acuff G.R. Lactic acid sprays reduce bacterial pathogens on cold beef carcass surfaces and in subsequently produced ground beef. Journal of Food Protection 2001, 64(1):58-62.
17. Centre for Infectious Disease Prevention and Control, Public Health Agency of Canada Notifiable diseases on-line 2005, Available at, Date last accessed 05.10.10. http://dsol-smed.phac-aspc.gc.ca/dsol-smed/cgi-bin/ndischart2?DATA_TYPE=R&YEAR_FROM=96&YEAR_TO=04&CAUSE=147&AREA=00&AGE=0&SEX=3&CTIME1=View+Chart.
18. Deeks J.J., Higgins J.P.T., Altman D.G. Analysing data and undertaking meta-analyses. Cochrane handbook for systematic reviews of interventions 2008, Available at, Version 5.0.1, The Cochrane Collaboration, Date last accessed 10.06.11. http://www.cochrane-handbook.org, J.P.T. Higgins, S. Green (Eds.).
19. DerSimonian R., Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemporary Clinical Trials 2007, 28:105-114.
20. Dickson J.S., Anderson M.E. Microbiological decontamination of food animal carcasses by washing and sanitizing systems: a review. Journal of Food Protection 1992, 55(2):133-140.
21. Dorsa W.J. New and established carcass decontamination procedures commonly used in the beef-processing industry. Journal of Food Protection 1997, 60(9):1146-1151.
22. Dorsa W.J., Cutter C.N., Siragusa G.R. Evaluation of six sampling methods for recovery of bacteria from beef carcass surfaces. Letters in Applied Microbiology 1996, 22(1):39-41.
23. Dorsa W.J., Cutter C.N., Siragusa G.R. Effectiveness of a steam-vacuum sanitizer for reducing Escherichia coli O157:H7 inoculated to beef carcass surface tissue. Letters in Applied Microbiology 1996, 23(1):61-63.
24. Dorsa W.J., Cutter C.N., Siragusa G.R., Koohmaraie M. Microbial decontamination of beef and sheep carcasses by steam, hot water spray washes, and a steam-vacuum sanitizer. Journal of Food Protection 1996, 59(2):127-135.
25. Duffy, G., Garvey, P., Wasteson, Y., McDowell, D., & Coia, J. (2001). Special issue: control of verocytotoxigenic E. coli. In Proceedings of conference organized as part of an EU concerted action on verocytotoxigenic E. coli (CT98-3935), September 6-8th 2000, Oslo, Norway. International Journal of Food Microbiology, 66(1/2), 1-129.
26. Duval S., Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000, 56:455-463.
27. Eblen D.R., Levine P., Rose B.E., Saini P., Mageau R., Hill W.E. Nationwide microbiological baseline data collected by sponge sampling during 1997 and 1998 for cattle, swine, turkeys, and geese. Journal of Food Protection 2005, 68(9):1848-1852.
28. Edwards J.R., Fung D.Y.C. Prevention and decontamination of Escherichia coli O157:H7 on raw beef carcasses in commercial beef abattoirs. The Journal of Rapid Methods and Automation in Microbiology 2006, 14(1):1-95.
29. Egger M., Davey Smith G., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315(7109):629-634.
30. Farrar, A. M. (2009). The application of research synthesis methods for evaluating primary research on Salmonella in broiler chickens. Master's thesis. Available at Date last accessed 12.09.11. http://www.collectionscanada.gc.ca/obj/thesescanada/vol2/002/MR56718.PDF.
31. Food Science Australia Organic acids 2006, Available at, Date last accessed 25.02.11. http://www.meatupdate.csiro.au/new/Organic%20Acids.pdf.
32. Friedrich J.O., Adhikari N.K., Beyene J. Inclusion of zero total event trials in meta-analyses maintains analytic consistency and incorporates all available data. BMC Medical Research Methodology 2007, 7(5):1-6. 10.1186/1471-2288-7-5.
33. Gill C. Visible contamination on animals and carcasses and the microbiological conditions of meat. Journal of Food Protection 2004, 67(2):413-419.
34. Gill C.O., Bandoni M. The effects of hot water pasteurizing treatments on the appearance of pork and beef. Meat Science 1997, 46(1):77-87.
35. Gill C.O., Bryant J. The effects on product of a hot water pasteurizing treatment applied routinely in a commercial beef carcass dressing process. Food Microbiology 2000, 17(5):495-504.
36. Gill C.O., Bryant J., Bedard D. The effects of hot water pasteurizing treatments on the appearances and microbiological conditions of beef carcass sides. Food Microbiology 1999, 16(3):281-289.
37. Gill C.O., Bryant J., Landers C. Identification of critical control points for control of microbiological contamination in processes leading to the production of ground beef at a packing plant. Food Microbiology 2003, 20(6):641-650.
38. Gill C.O., Jones T. Microbiological sampling of carcasses by excision or swabbing. Journal of Food Protection 2000, 63(2):167-173.
39. Gill C.O., Landers C. Microbial effects of carcass decontaminating treatments at four beef packing plants. Meat Science 2003, 65(3):1005-1011.
40. Gill C.O., McGinnis J.C., Bryant J. Microbial contamination of meat during the skinning of beef carcass hindquarters at three slaughtering plants. International Journal of Food Microbiology 1998, 42:175-184.
41. Heuvelink A.E., Roessink G.L., Bosboom K., de Boer E. Zero tolerance for fecal contamination of carcasses as a tool in the control of 0157 VTEC infections. International Journal of Food Microbiology 2001, 66(1-2):13-20.
42. Cochrane handbook for systematic reviews of interventions 2011, Version 5.1.0 [updated March 2011], The Cochrane Collaboration, Available at, Date last accessed 13.06.11. http://www.cochrane-handbook.org/, J.P.T. Higgins, S. Green (Eds.).
43. Higgins JP.T., Thompson S.G., Deeks J.J., Altman D.G. Measuring inconsistency in meta-analyses. BMJ 2003, 327(7414):557-560.
44. Higgins JP.T., White I.R., Anzures-Cabrera J. Meta-analysis of skewed data: combining results reported on log-transformed or raw scales. Statistics in Medicine 2008, 27(29):6072-6092.
45. Hoffmann L., Webb E.C. 54th International congress of meat science and technology (54th ICoMST), Cape Town, South Africa, 10-15 August 2008. Meat Science 2008, 80(1):1-149.
46. Hunt M.C. 51st international congress of meat science and technology (51st ICoMST), Baltimore, USA, 7-12 August 2005. Meat Science 2005, 71(1):1-217.
47. IDF/FAO/WHO symposium on revolution in food safety management, 13-15 February 2008, Bali, Indonesia.
48. International Dairy Federation. (2009). A revolution in food safety management. Bulletin of the International Dairy Federation (no. 433, 108 pp.).
49. International Meat and Poultry HACCP Alliance Generic HACCP model for beef slaughter 1996, Available at, Date last accessed 13.06.11. http://haccpalliance.org/sub/haccpmodels/beefslaughter.pdf.
50. Ioannidis JP.A., Trikalinos T.A. The appropriateness of asymmetry tests for publication bias in meta-analysis: a large survey. Canadian Medical Association Journal 2007, 176(8):1091-1096.
51. Karmali M.A., Petric M., Steele B.T., Lim C. Sporadic cases of hemolytic uremic syndrome associated with fecal cytotoxin and cytotoxin-producing Escherichia coli. Lancet 1983, 1(8325):619-620.
52. Li J., McLandsborough L.A. The effects of the surface charge and hydrophobicity of Escherichia coli on its adhesion to beef muscle. International Journal of Food Microbiology 1999, 53(2-3):185-193.
53. Mederos Silveira, A. E. (2010). Epidemiological studies of gastrointestinal nematodes in sheep flocks in Ontario and Quebec, Canada (p. 234). PhD thesis, University of Guelph, Guelph, Ont. Available at Date last accessed 16.09.11. http://proquest.umi.com/pqdlink?Ver=1%26Exp=09-14-2016%26FMT=7%26DID=2111278131%26RQT=309%26attempt=1%26cfc=1.
54. Miller A.J., Smith J.L., Buchanan R.L. Factors affecting the emergence of new pathogens and research strategies leading to their control. Journal of Food Safety 1998, 18(4):243-263.
55. Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 2009, 6(7):e1000097. PRISMA Group.
56. Nou X., Rivera-Betancourt M., Bosilevac J.M., Wheeler T.L., Shackelford S.D., Gwartney B.L., et al. Effect of chemical dehairing on the prevalence of Escherichia coli O157:H7 and the levels of aerobic bacteria and Enterobacteriaceae on carcasses in a commercial beef processing plant. Journal of Food Protection 2003, 66(11):2005-2009.
57. Nutsch A.L., Phebus R.K., Riemann M.J., Schafer D.E., Boyer J.E., Wilson R.C., et al. Evaluation of a steam pasteurization process in a commercial beef processing facility. Journal of Food Protection 1997, 60(5):485-492.
58. Phillips C.A. The epidemiology, detection and control of Escherichia coli O157. Journal of the Science of Food and Agriculture 1999, 79:1367-1381.
59. Rangel J.M., Sparling P.H., Crowe C., Griffin P.M., Swerdlow D.L. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerging Infectious Diseases 2005, 11(4):603-609.
60. Ravel A., Greig J., Tinga C., Todd E., Campbell G., Cassidy M., et al. Exploring historical Canadian foodborne outbreak datasets for human illness attribution. Journal of Food Protection 2009, 72(9):1963-1976.
61. Retzlaff D., Phebus R., Kastner C., Marsden J. Establishment of minimum operational parameters for a high-volume static chamber steam pasteurization system (SPS 400-SC) for beef carcasses to support HACCP programs. Foodborne Pathogens and Disease 2005, 2(2):146-151.
62. Riley L.W., Remis R.S., Helgerson S.D., McGee H.B., Wells J.G., Davis B.R., et al. Haemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine 1983, 308:681-684.
63. Russell J.B., Diez-Gonzalez F., Jarvis G.N. Invited review: effects of diet shifts on Escherichia coli in cattle. Journal of Dairy Science 2000, 83(4):863-873.
64. Sargeant J.M., Amezcua M.R., Rajíc A., Waddell L. Pre-harvest interventions to reduce the shedding of E. coli O157 in the faeces of weaned domestic ruminants: a systematic review. Zoonoses and Public Health 2007, 54(6-7):260-277.
65. Sargeant J.M., Rajić A., Read S., Ohlsson A. The process of systematic review and its application in agri-food public-health. Preventive Veterinary Medicine 2006, 75(3-4):141-151.
66. Simpson C.A., Ransom J.R., Scanga J.A., Belk K.E., Sofos J.N., Smith G.C. Changes in microbiological populations on beef carcass surfaces exposed to air- or spray-chilling and characterization of hot box practices. Food Protection Trends 2006, 26(4):226-235.
67. Smith, G. C., Sofos, J. N., Belk, K. E., Scanga, J. A., & Tatum, J. D. (2000). Pathogen contamination of cattle and beef challenges and opportunities in process control. 21st World Buiatrics congress, Punta Del Este, Uruguay.
68. Snedeker K.G., Campbell M., Sargeant J.M. A systematic review of vaccinations to reduce the shedding of Escherichia coli O157 in the faeces of domestic ruminants. Zoonoses and Public Health 2011, Article first published online: 10 Jul 2011. 10.1111/j.1863-2378.2011.01426.x.
69. Støier S. 55th International congress of meat science and technology (55th ICoMST), Copenhagen, Denmark, 16-21 August 2009. Meat Science 2010, 84(2):1-313.
70. Stopforth J.D., Lopes M., Shultz J.E., Miksch R.R., Samadpour M. Location of bung bagging during beef slaughter influences the potential for spreading pathogen contamination on beef carcasses. Journal of Food Protection 2006, 69(6):1452-1455.
71. Stringer M. Food safety objectives - role in microbiological food safety management. Food Control 2005, 16(9):775-794.
72. Sumner S.S., Albrecht J.A. Implementation of food safety/HACCP training for small food processors: a pilot study in Nebraska. Dairy Food and Environmental Sanitation 1995, 15(7):424-429.
73. 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(5):378-382.
74. Thomas M.K., Majowicz S.E., Sockett P.N., Fazil A., Pollari F., Doré K., et al. Estimated numbers of community cases of illness due to Salmonella, Campylobacter and verotoxigenic Escherichia coli: pathogen-specific community rates. The Canadian Journal of Infectious Diseases & Medical Microbiology 2006, 17(4):229-234.
75. Troy D.J., Buckley J., Byrne B., Pearce R. 52nd International congress of meat science and technology (52nd ICoMST), Dublin, Ireland, 13-18 August 2006. Meat Science 2006, 74(1):1-229.
76. United States Department of Agriculture Pathogen reduction; hazard analysis and critical control point (HACCP) systems; final rule. Federal Register 1996, 61:38806-38989. Available at, Date last accessed 03.02.11. http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/93-016F.pdf.
77. Uruguayan Veterinary Association, & World Association for Buiatrics. Abstracts, 21 world buiatrics congress, 27 Uruguayan buiatrics journey, 4-8 December 2000, Punta del Este, Uruguay (184 pp.).
78. Vivas-Alegre L., Buncic S. Potential for use of hide-carcass microbial counts relationship as an indicator of process hygiene performance of cattle abattoirs. Food Protection Trends 2004, 24(11):814-820.
79. Weingold S.E., Guzewich J.J., Fudala J.F. Use of foodborne disease data for HACCP risk assessment. Journal of Food Protection 1994, 57(9):820-830.
80. Wilhelm B., Rajić A., Greig J.D., Waddell L., Harris J. The effect of hazard analysis critical control point programs on microbial contamination of carcasses in abattoirs: a systematic review of published data. Foodborne Pathogens and Disease 2011, 8(9):949-960.
81. 14th World Congress of Food Science & Technology. (2008). (721 pp.).
82. Zhou G. 53rd International congress of meat science and technology (53rd ICoMST), Beijing, China, 5-10 August 2007. Meat Science 2007, 77(1):1-147.