Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T17:37:39.923Z Has data issue: false hasContentIssue false
  • English
  • Français

Systematic review of the magnitude of change in prevalence and quantity of Salmonella after administration of pathogen reduction treatments on pork carcasses

Published online by Cambridge University Press:  18 July 2016

Sarah C. Totton ,
Julie M. Glanville ,
Rungano S. Dzikamunhenga ,
James S. Dickson  and
Annette M. O'Connor
Sarah C. Totton
Affiliation:
63 College Avenue West, Guelph ON N1G 1S1, Canada
Julie M. Glanville
Affiliation:
York Health Economics Consortium Ltd., Level 2 Market Square, University of York, York, YO10 5NH, UK
Rungano S. Dzikamunhenga
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
James S. Dickson
Affiliation:
Department of Animal Science, Iowa State University, Ames, IA 50011, USA
Annette M. O'Connor*
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
*
*Corresponding author. E-mail: oconnor@iastate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

In this systematic review, we summarized change in Salmonella prevalence and/or quantity associated with pathogen reduction treatments (washes, sprays, steam) on pork carcasses or skin-on carcass parts in comparative designs (natural or artificial contamination).

Methods:

In January 2015, CAB Abstracts (1910–2015), SCI and CPCI–Science (1900–2015), Medline® and Medline® In-Process (1946–2015) (OVIDSP), Science.gov, and Safe Pork (1996–2012) were searched with no language or publication type restrictions. Reference lists of 24 review articles were checked. Two independent reviewers screened 4001 titles/abstracts and assessed 122 full-text articles for eligibility. Only English-language records were extracted.

Results:

Fourteen studies (5 in commercial abattoirs) were extracted and risk of bias was assessed by two reviewers independently. Risk of bias due to systematic error was moderate; a major source of bias was the potential differential recovery of Salmonella from treated carcasses due to knowledge of the intervention. The most consistently observed association was a positive effect of acid washes on categorical measures of Salmonella; however, this was based on individual results, not a summary effect measure.

Conclusion:

There was no strong evidence that any one intervention protocol (acid temperature, acid concentration, water temperature) was clearly superior to others for Salmonella control.

Keywords

carcassinterventionporkSalmonellasystematic review
Type
Review Article
Information
Animal Health Research Reviews , Volume 17 , Special Issue 1: Systematic Reviews , June 2016 , pp. 39 - 59
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Biemuller, GW, Carpenter, JA and Reynolds, AE (1973). Reduction of bacteria on pork carcasses. Journal of Food Science 38: 261–263.CrossRefGoogle Scholar
Bolton, DJ, Pearce, RA, Sheridan, JJ, Blair, IS, McDowell, DA and Harrington, D (2002). Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. Journal of Applied Microbiology 92: 893–902.CrossRefGoogle ScholarPubMed
Christiansen, P, Krag, R and Aabo, S (2009). Effect of hot water and lactic acid decontamination on Escherichia coli, Salmonella Typhimurium and Yersinia enterocolitica on pork. Eighth International Symposium on the Epidemiology and Control of Foodborne Pathogens in Pork, Ames, IA, USA, pp. 253–257.CrossRefGoogle Scholar
Davies, RH, McLaren, IM and Bedford, S (1999). Distribution of Salmonella contamination in two pig abattoirs. Proceedings of the 3rd International Symposium on the Epidemiology and Control of Salmonella in Pork, Washington, DC, USA, pp. 267–272.Google Scholar
EFSA (European Food Safety Authority) (2011). Scientific opinion on the evaluation of the safety and efficacy of lactic acid for the removal of microbial surface contamination of beef carcasses, cuts and trimmings. EFSA Journal 9: 2317.Google Scholar
Eggenberger-Solorzano, L, Neibuhr, SE, Acuff, GR and Dickson, JS (2002). Hot water and organic acid interventions to control microbiological contamination on hog carcasses during processing. Journal of Food Protection 65: 1248–1252.Google Scholar
Egger, M, Smith, GD and Altman, D (2008). Systematic Reviews in Health Care: Meta-Analysis in Context, Second Edition. London, UK: BMJ Publishing Group. [Available online at http://onlinelibrary.wiley.com/book/10.1002/9780470693926;jsessionid=564B984DEDE045F354942CD9B2DD28C8.f01t03] Last accessed 3 March 2016.Google Scholar
Epling, LK (1987). Reduction of Salmonella and Campylobacter on pork carcasses using lactic acid as a decontaminant. MS Thesis, University of Georgia, Athens, GA, USA.Google Scholar
Epling, LK, Carpenter, JA and Blankenship, LC (1993). Prevalence of Campylobacter spp. and Salmonella spp. on pork carcasses and the reduction effected by spraying with lactic acid. Journal of Food Protection 56: 536–537, 540.CrossRefGoogle ScholarPubMed
Fabrizio, KA and Cutter, CN (2004). Comparison of electrolyzed oxidizing water with other antimicrobial interventions to reduce pathogens on fresh pork. Meat Science 68: 463–468.Google Scholar
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) (2015). Interventions for the Control of Nontyphoidal Salmonella spp. in Beef and Pork. Report of a Joint FAO/WHO Expert Meeting, 28 September - 2 October 2015, FAO, Rome, Italy. [Available online at http://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https://%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FMeetings%252FCX-712-47%252FSalmonella%2Bexpert%2Bmeeting%2Breport%2B-%2BOct%2B20%2B%25282%2529.pdf] Google Scholar
FSIS/USDA (Food Safety and Inspection Service/United States Department of Agriculture) (1998). Self-instruction guide for collecting raw meat and poultry product samples for Salmonella analysis. FSIS Directive 10,230.5, Amend 1. [Available online at http://www.fsis.usda.gov/OPPDE/rdad/FSISDirectives/10230-5.pdf] Last accessed 18 September 2015.Google Scholar
Hamilton, D, Holds, G, Lorimer, M, Kiermeier, A, Kidd, C, Slade, J and Pointon, A (2010). Slaughterfloor decontamination of pork carcases with hot water or acidified sodium chlorite – a comparison in two Australian abattoirs. Zoonoses Public Health 57(Suppl 1): 16–22. doi:10.1111/j.1863-2378.2010.01359.x.Google Scholar
Hernandez, M, Gomez-Laguna, J, Luque, I, Herrera-Leon, S, Maldonado, A, Reguillo, L and Astorga, RJ (2013). Salmonella prevalence and characterization in a free-range pig processing plant: tracking in trucks, lairage, slaughter line and quartering. International Journal of Food Microbiology 162: 48–54.CrossRefGoogle Scholar
Higgins, JPT, Altman, DG and Sterne, JAC (2011). Chapter 8: Assessing risk of bias in included studies. In: Higgins, JPT and Green, S (eds) Cochrane Handbook for Systematic Reviews of Interventions, Version 5.1.0 (updated March 2011). The Cochrane Collaboration, [Available online at http://www.cochrane-handbook.org]Google Scholar
Hricova, D, Stephan, R and Zweifel, C (2008). Electrolyzed water and its application in the food industry. Journal of Food Protection 71: 1934–1947.Google Scholar
Lawson, LG, Jensen, JD, Christiansen, P and Lund, M (2009). Cost-effectiveness of Salmonella reduction in Danish abattoirs. International Journal of Food Microbiology 134: 126–132.Google Scholar
Loretz, M, Stephan, R and Zweifel, C (2011). Antibacterial activity of decontamination treatments for pig carcasses. Food Control 22: 1121–1125.CrossRefGoogle Scholar
Machado, AR, Gouveia, FC, Picinin, LCA, Kich, JD, de Cardoso, MR I and Ferraz, SM (2013). Microbiological and physicochemical evaluation of pork leg treated with organic acids and/or steam under pressure in the control of surface contamination by Salmonella Typhimurium. Ciência Animal Brasileira, Goiânia 14: 345–351.Google Scholar
Midgley, J and Small, A (2006). Review of new and emerging technologies for red meat safety. North Sydney, NSW, Australia: Meat & Livestock Australia Ltd. [Available online at http://www.meatupdate.csiro.au/new/Review%20of%20new%20and%20emerging%20technlogies%20for%20red%20meat%20safety.pdf] Last accessed 30 December 2015.Google Scholar
Milios, K, Drosinos, EH and Zoiopoulos, PE (2014). Carcass decontamination methods in slaughterhouses: a review. Journal of the Hellenic Veterinary Medical Society 65: 65–78.CrossRefGoogle Scholar
Miller, GY, Liu, X, McNamara, PE and Barber, DA (2005). Influence of Salmonella in pigs preharvest and during pork processing on human health costs and risks from pork. Journal of Food Protection 68: 1788–1798.Google Scholar
Mohr, D, Liberati, A, Tetzlaff, J and Altman, DG (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLoS Medicine 6: e1000097.Google Scholar
Morild, RK, Christiansen, P, Sørensen, AH, Nonboe, U and Aabo, S (2011a). Inactivation of pathogens on pork by steam-ultrasound treatment. Journal of Food Protection 74: 769–775.Google Scholar
Morild, RK, Olsen, JE and Aabo, S (2011b). Change in attachment of Salmonella Typhimurium, Yersinia enterocolitica, and Listeria monocytogenes to pork skin and muscle after hot water and lactic acid decontamination. International Journal of Food Microbiology 145: 353–358.Google Scholar
Morris, CA, Lucia, LM, Savell, JW and Acuff, GR (1997). Trisodium phosphate treatment of pork carcasses. Journal of Food Science 62: 402–405.Google Scholar
O'Connor, AM, Sargeant, JM, Gardner, IA, Dickson, JS, Torrence, ME, Dewey, CE, Dohoo, IR, Evans, RB, Gray, JT, Greiner, M, Keefe, G, Lefebvre, SL, Morley, PS, Ramirez, A, Sischo, W, Smith, DR, Snedeker, K, Sofos, J, Ward, MP and Wills, R (2010). The REFLECT statement: methods and processes of creating reporting guidelines for randomized controlled trials for livestock and food safety. Preventive Veterinary Medicine 93: 11–18.CrossRefGoogle ScholarPubMed
Painter, JA, Hoekstra, RM, Ayers, T, Tauxe, RV, Braden, CR, Angulo, FJ and Griffin, PM (2013). Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerging Infectious Diseases 19. doi:10.3201/eid1903.111866. Table 4. [Available online at http://wwwnc.cdc.gov/eid/article/19/3/11-1866-t4] Last accessed 29 December 2015.CrossRefGoogle ScholarPubMed
Pearce, RA, Bolton, DJ, Sheridan, JJ, McDowell, DA, Blair, IS and Harrington, D (2004). Studies to determine the critical control points in pork slaughter hazard analysis and critical control point systems. International Journal of Food Microbiology 90: 331–339.Google Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org Google Scholar
Schünemann, H, Brożek, J, Guyatt, G and Oxman, A (Updated October 2013). Handbook for Grading the Quality of Evidence and the Strength of Recommendations using the GRADE Approach. Hamilton, ON, Canada: The GRADE Working Group. [Available online at http://www.guidelinedevelopment.org/handbook] Last accessed 26 June 2015.Google Scholar
Schwarzer, G (2015). meta: General Package for Meta-Analysis. R package version 4.2-0. [Available at http://CRAN.R-project.org/package=metareference] for RGoogle Scholar
Totton, S, Glanville, J, Dzikamunhenga, R, Dickson, J and O'Connor, A (2015). Systematic review of the magnitude of change in the prevalence of Salmonella and the quantity of Salmonella after administration of pathogen reduction treatments on pork carcasses: interim summary, p 29–31. Eleventh International Conference on the Epidemiology and Control of Biological, Chemical and Physical Hazards in Pigs and Pork, Porto, Portugal.Google Scholar
Trivedi, S, Reynolds, AE and Chen, J (2007). Use of a commercial household steam cleaning system to decontaminate beef and hog carcasses processed by four small or very small meat processing plants in Georgia. Journal of Food Protection 70: 635–640.CrossRefGoogle ScholarPubMed
van Netten, P, Huls in't Veld, J and Mossel, DAA (1994). An in-vitro meat model for the immediate bactericidal effect of lactic acid decontamination on meat surfaces. Journal of Applied Bacteriology 76: 49–54.CrossRefGoogle ScholarPubMed
van Netten, P, Mossel, DAA and Huis In ‘t Veld, J (1995). Lactic acid decontamination of fresh pork carcasses: a pilot plant study. International Journal of Food Microbiology 25: 1–9.CrossRefGoogle ScholarPubMed
WHO (World Health Organization) (2013). Salmonella (non-typhoidal) Fact Sheet Number 139. [Available online at http://www.who.int/mediacentre/factsheets/fs139/en/] Accessed 22 June 2015.Google Scholar
Young, I, Wilhelm, B, Cahill, S, Nakagawa, R, Desmarchelier, P and Rajić, A (2015). Rapid Systematic Review of the Efficacy of Interventions to Control Salmonella in Pork and Beef. Rome, Italy: World Health Organization/Food and Agricultural Organization of the United Nations.Google Scholar
Supplementary material: File

Totton supplementary material

Totton supplementary material 1

Download Totton supplementary material(File)
File 101.8 KB