Ozone application has been suggested as an additional measure to the slaughter animals under hygiene programs. In this study, we determined the efficacy of gaseous ozone applied to pig carcasses during chilling (16 h at 2–5°C). Forty carcasses were allocated to each treatment: control, without ozone application (T1) and 5 ppm gaseous ozone application (T2), divided in two 4-h periods. The carcasses were sampled before and after chilling. The average counts of total aerobic mesophilic (TAM) bacteria before chilling were not different (p = 0.55) between T1 and T2. In turn, after chilling, the ozone-treated carcasses had significantly reduced about 0.4 colony-forming units (CFU)/cm2 of TAM counts (p < 0.001) than the control carcasses. No significant reduction was observed in the number of carcasses positive for Listeria sp. and Escherichia coli after gaseous ozone treatment; while a tendency (p = 0.08) of lower number of Salmonella positive carcasses in T2 was observed. Common macrorestriction (pulsed-field gel electrophoresis) patterns of S. enterica were observed in the carcasses before and after chilling. Pork samples from treated and untreated carcasses with ozone showed no lipid oxidation or altered color and pH. The results indicate that the gaseous ozone in the tested protocol is effective in reducing TAM populations, but not effective in decreasing the number of carcasses positive for E. coli and Listeria sp. Regarding Salmonella, the tendency of positive carcasses reduction may encourage further studies by testing other protocols of gaseous ozone application inside the chilling chamber.
AyranciUGOzunluOErgezerHKaracaH. (2019).
Effects of ozone treatment on microbiological quality and physicochemical properties of turkey breast meat. Ozone: Science & Engineering42(1): 95–103.
2.
BoltonDJPearceRASheridanJJBlairISMcDowellDAHarringtonD. (2002).
Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. Journal of Applied Microbiology92(5): 893–902.
3.
BonardiSBruiniIBolzoniLCozzolinoPPierantoniMBrindaniF, et al. (2017).
Assessment of Salmonella survival in dry-cured Italian salami. International Journal of Food Microbiology262(September): 99–106.
4.
BrodowskaANowakAKondratiuk-JanyskaAPiątkowskiMŚmigielskiK. (2017).
Modelling the ozone-based treatments for inactivation of microorganisms. International Journal of Environmental Research and Public Health14(10): 1196.
5.
Brasil (1995). Portaria 711 de 01 de novembro de 1995. Aprova as normas técnicas de instalações e equipamentos para abate e industrialização de suínos. Diário Oficial da União de 03/11/95 seção 1 página 17625. Brasília.
6.
CamposCARodriguezOLosadaVAubourgSPBarros-VelázquezJ. (2005).
Effects of storage in ozonised slurry ice on the sensory and microbial quality of sardine (Sardina pilchardus). International Journal of Food Microbiology103: 121–130.
7.
CandiaSMoreaMBaruzziF. (2015).
Eradication of high viable loads of Listeria monocytogenes contaminating food-contact surfaces. Frontiers in Microbiology6: 733.
8.
CanoCMenesesYChavesB. (2019).
Ozone-based interventions to improve the microbiological safety and quality of poultry carcasses and parts: A review. Journal of Food Protection82(6): 940–947.
9.
CantalejoMJZouaghiFPérez-ArnedoI. (2016).
Combined effects of ozone and freeze-drying on the shelf-life of broiler chicken meat. LWT – Food Science and Technology68: 400–407.
10.
Coll CárdenasFAndrésSGiannuzziLZaritzkyN. (2011).
Antimicrobial action and effects on beef quality attributes of a gaseous ozone treatment at refrigeration temperatures. Food Control22(8): 1442–1447.
11.
Centers for Disease Control and Prevention (2014). PulseNet pathogens & protocols: PFGE. Protocols. Atlanta. Available at: www.cdc.gov/pulsenet/pathogens/index.html (accessed 22 April 2021).
12.
CortesiMLSarnoECostanzoNFerranteSSantoroA. (2011).
Decontaminazione mediante ozono di carcasse di pollo refrigerate. Italian Journal of Food Safety1(1): 51–54.
13.
CosansuSAyhanK. (2012).
Effects of lactic and acetic acid on survival of Salmonella enteritidis during refrigerated and frozen storage of chicken meats. Food and Bioprocess Technology5(1): 372–377.
14.
CullenPJNortonT. (2012). Ozone sanitation in food industry. In: DonnelCOTiwariBKCullenPJ, et al. (eds) Ozone in Food Processing.
New Jersey:
Blackwell Publishing, pp.163–176.
15.
DelhalleLDe SadeleerLBollaertsKFarnirFSaegermanCKorsakN, et al. (2008).
Risk factors for Salmonella and hygiene indicators in the 10 largest Belgian pig slaughterhouses. Journal of Food Protection71(7): 1320–1329.
16.
FabrizioKASharmaRRDemirciACutterCN. (2002).
Comparison of electrolyzed oxidizing water with various antimicrobial interventions to reduce Salmonella species on poultry. Poultry Science81: 1598–1605.
17.
FernándezJPérez-AlvarezJAFernández-LopezJA. (1997).
Thiobarbituric acid test for monitoring lipid oxidation in meat. Food Chemistry59(3): 345–353.
18.
FerrariRGRosarioDKACunha-NetoAManoSBFigueiredoEESConte-JuniorCA. (2019).
Worldwide epidemiology of Salmonella serovars in animal-based foods: A meta-analysis. Applied and Environmental Microbiology85(14): e00591–19.
19.
Food and Agriculture Organization of the United Nations and World Health Organization (2016). Interventions for the control of non-typhoidal Salmonella spp. in beef and pork: meeting report and systematic review. Microbiological risk assessment series 30, Rome.
20.
GiménezBGraiverNGiannuzziLZaritzkyN. (2021).
Treatment of beef with gaseous ozone: Physicochemical aspects and antimicrobial effects on heterotrophic microflora and listeria monocytogenes. Food Control121: 107602.
21.
ISO 17604:2003 (2003). Microbiology of food and animal feeding stuffs – Carcass sampling for microbiological analysis.
22.
JakschDMargesinRMikovinyTSkalnyJDHartungenESchinnerF, et al. (2004).
The effect of ozone treatment on the microbial contamination of pork meat measured by detecting the emissions using PTR-MS and by enumeration of microorganisms. International Journal of Mass Spectrometry239(2–3): 209–214.
23.
JulsonJLMuthukumarappanKHenningDI. (2001). Effectiveness of ozone for controlling Listeria monocytogenes in ready to eat cured ham. Report NPPC Project #99-221.
Brookings, SD:
South Dakota State University.
24.
KalchayanandNBosilevacJMKingDAWheelerTL. (2020).
Evaluation of UVC radiation and a UVC-Ozone combination as fresh beef interventions against Shiga toxin-producing Escherichia coli, Salmonella, and Listeria monocytogenes and their effects on beef quality. Journal of Food Protection83(9): 1520–1529.
25.
KhadreMAYousefAEKimJG. (2001).
Microbiological aspects of ozone applications in food: A review. Journal of Food Science66(9): 1242–1252.
26.
KimJYousefAEDaveS. (1999).
Application of ozone for enhancing the microbiological safety and quality of foods: a review. Journal of Food Protection62: 1071–1087.
27.
MasottiFValloneLRanziniSSilvetTMorandiSBrascaM. (2019).
Effectiveness of air disinfection by ozonation or hydrogen peroxide aerosolization in dairy environments. Food Control97: 32–38.
28.
MegahedAAldridgeBLoweJ. (2020).
Antimicrobial efficacy of aqueous ozone and ozone–lactic acid blend on Salmonella-contaminated chicken drumsticks using multiple sequential soaking and spraying approaches. Frontiers in Microbiology11: 593911.
29.
MillerFASilvaCLMBrandãoTRS. (2013).
A review on ozone-based treatments for fruit and vegetables preservation. Food Engineering Reviews5(2): 77–106.
30.
MorandiSBrascaMLodiRBattelliG. (2009).
Use of ozone to control Listeria monocytogenes in various types of cheese. Scienza e Tecnica Lattiero-Casearia60: 211–215.
31.
MuthukumarAMuthuchamyM. (2013).
Optimization of ozone in gaseous phase to inactivate Listeria monocytogenes on raw chicken samples. Food Research International54(1): 1128–1130.
32.
MuhlisinMUtamaDTLeeJHChoiJHLeeSK. (2016).
Effects of gaseous ozone exposure on bacterial counts and oxidative properties in chicken and duck breast meat. Korean Journal for Food Science of Animal Resources36: 405–411.
33.
National Institute for Occupational Safety and Health (2014). Ozone. Immediately dangerous to life or healthy concentrations. Available at: www.cdc.gov/niosh/idlh/10028156.html (accessed 22 April 2021).
34.
PascualALlorcaICanutA. (2007).
Use of ozone in food industries for reducing the environmental impact of cleaning and disinfection activities. Trends in Food Science & Technology18: S29–S35.
35.
PerryJJYousefAE. (2011).
Decontamination of raw foods using ozone-based sanitization techniques. Annual Review Food Science and Technology2: 281–298.
36.
CPiachinTTrachooN. (2011).
Effect of ozone and potassium lactate on lipid oxidation and survival of Salmonella typhimurium on fresh pork. Pakistan Journal of Biological Sciences14(3): 236–240. [CrossRef][10.3923/pjbs.2011.236.240]
37.
QuinnPJMarkeyBKLeonardFCHartiganPJFanningSFitzpatrickES. (2011). Veterinary Microbiology and Microbial Disease.
New Jersey:
Wiley-Blackwell.
38.
ReitznerováAŠulekováMNagyJMarcinčákSSemjonBČertíkM, et al. (2017).
Lipid peroxidation process in meat and meat products: A comparison study of malondialdehyde determination between modified 2-thiobarbituric acid spectrophotometric method and reverse-phase High-Performance liquid chromatography. Molecules22(11): 1988.
39.
TrindadeMAKushidaMMMontes VillanuevaMDdos Santos PereiraDULins de OliveiraCE. (2012).
Comparison of ozone and chlorine in low concentrations as sanitizing agents of chicken carcasses in the water immersion chiller. Journal of Food Protection75: 1139–1143.
40.
Van der WalPGBolinkAHMerkusGSM. (1988).
Differences in quality characteristics of normal, PSE and DFD pork. Meat Science24(1): 79–84.
41.
WarnerR. (2014). Measurement of meat quality – Measurements of water holding capacity and color: Objective and subjective. In: DikemanMDevineC (eds) Encyclopedia of Meat Sciences.
Vol. 1, 2nd ed.
UK:
Academic Press, pp.164–171.
42.
WenjiaoFYongkuiZYunchuanCJunxiuSYuwenY. (2014).
TBARS predictive models of pork sausages stored at different temperatures. Meat Science96(1): 1–4.
43.
WheatleyPGiotisESMcKevittAI. (2014).
Effects of slaughtering operations on carcass contamination in an Irish pork production plant. Irish Veterinary Journal67(1): 1.
44.
World Health Organization (2015). WHO estimates of the global burden of foodborne diseases: Foodborne disease burden epidemiology reference group 2007–2015.
Geneva:
World Health Organization.
