Systematic Review and Meta-Analysis of the Efficacy of Interventions Applied during Primary Processing to Reduce Microbial Contamination on Pig Carcasses

Nevijo Zdolec; Aurelia Kotsiri; Kurt Houf; Avelino Alvarez-Ordóñez; Bojan Blagojevic; Nedjeljko Karabasil; Morgane Salines; Dragan Antic

doi:10.3390/foods11142110

Systematic Review and Meta-Analysis of the Efficacy of Interventions Applied during Primary Processing to Reduce Microbial Contamination on Pig Carcasses

Foods. 2022 Jul 15;11(14):2110. doi: 10.3390/foods11142110.

Authors

Nevijo Zdolec¹, Aurelia Kotsiri², Kurt Houf³, Avelino Alvarez-Ordóñez⁴, Bojan Blagojevic⁵, Nedjeljko Karabasil⁶, Morgane Salines⁷, Dragan Antic²

Affiliations

¹ Faculty of Veterinary Medicine, University of Zagreb, 10000 Zagreb, Croatia.
² Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool L69 3BX, UK.
³ Faculty of Veterinary Medicine, Department of Veterinary and Biosciences, Ghent University, 9820 Merelbeke, Belgium.
⁴ Institute of Food Science and Technology, Department of Food Hygiene and Technology, Universidad de León, 24004 León, Spain.
⁵ Faculty of Agriculture, Department of Veterinary Medicine, University of Novi Sad, 21000 Novi Sad, Serbia.
⁶ Faculty of Veterinary Medicine, University of Belgrade, Department of Food Hygiene and Technology, 11000 Belgrade, Serbia.
⁷ French Ministry of Agriculture, Office for Slaughterhouses and Cutting Plants, 75015 Paris, France.

Abstract

Interventions from lairage to the chilling stage of the pig slaughter process are important to reduce microbial contamination of carcasses. The aim of this systematic review and meta-analysis was to assess the effectiveness of abattoir interventions in reducing aerobic colony count (ACC), Enterobacteriaceae, generic Escherichia coli, and Yersinia spp. on pig carcasses. The database searches spanned a 30 year period from 1990 to 2021. Following a structured, predefined protocol, 22 articles, which were judged as having a low risk of bias, were used for detailed data extraction and meta-analysis. The meta-analysis included data on lairage interventions for live pigs, standard processing procedures for pig carcasses, prechilling interventions, multiple carcass interventions, and carcass chilling. Risk ratios (RRs) for prevalence studies and mean log differences (MDs) for concentration outcomes were calculated using random effects models. The meta-analysis found that scalding under commercial abattoir conditions effectively reduced the prevalence of Enterobacteriaceae (RR: 0.05, 95% CI: 0.02 to 0.12, I² = 87%) and ACC (MD: -2.84, 95% CI: -3.50 to -2.18, I² = 99%) on pig carcasses. Similarly, significant reductions of these two groups of bacteria on carcasses were also found after singeing (RR: 0.25, 95% CI: 0.14 to 0.44, I² = 90% and MD: -1.95, 95% CI: -2.40 to -1.50, I² = 96%, respectively). Rectum sealing effectively reduces the prevalence of Y. enterocolitica on pig carcasses (RR: 0.60, 95% CI: 0.41 to 0.89, I² = 0%). Under commercial abattoir conditions, hot water washing significantly reduced ACC (MD: -1.32, 95% CI: -1.93 to -0.71, I² = 93%) and generic E. coli counts (MD: -1.23, 95% CI: -1.89 to -0.57, I² = 61%) on pig carcasses. Conventional dry chilling reduced Enterobacteriaceae prevalence on pig carcasses (RR: 0.32, 95% CI: 0.21 to 0.48, I² = 81%). Multiple carcass interventions significantly reduced Enterobacteriaceae prevalence (RR: 0.11, 95% CI: 0.05 to 0.23, I² = 94%) and ACC on carcasses (MD: -2.85, 95% CI: -3.33 to -2.37, I² = 97%). The results clearly show that standard processing procedures of scalding and singeing and the hazard-based intervention of hot water washing are effective in reducing indicator bacteria on pig carcasses. The prevalence of Y. enterocolitica on pig carcasses was effectively reduced by the standard procedure of rectum sealing; nevertheless, this was the only intervention for Yersinia investigated under commercial conditions. High heterogeneity among studies and trials investigating interventions and overall lack of large, controlled trials conducted under commercial conditions suggest that more in-depth research is needed.

Keywords: Enterobacteriaceae; Yersinia; abattoir; aerobic colony count; chilling; generic E. coli; hot water washing; interventions; pig carcasses.

Grants and funding

This research received no external funding. The APC was funded by COST Action 18105 (Risk-based Meat Inspection and Integrated Meat Safety Assurance).