Abstract
Studies were undertaken to investigate the effect of different modified atmospheric packaging (MAP) gaseous combinations on Campylobacter and the natural microflora on poultry fillets. Skinless chicken fillets were stored in gaseous mixtures of 10%, 30%, 50%, 70% and 90% CO2 balanced with N2, 80:20% O2:N2 and 40:30:30% CO2:O2:N2 and control conditions (air) at 2 C. Samples were analysed periodically for (previously inoculated) Campylobacter, total viable counts (TVC) (mesophiles), TVC (psychrophiles), Enterobacteriaceae, Pseudomonas and lactic acid bacteria (LAB) over 17 days of storage. The carbon dioxide solubility was determined by monitoring the changes in the headspace volume over time using a buoyancy technique and performing calculations based on volumetric measurements and the Henry's constant. Henry's constant was also used to estimate the oxygen solubility in the chicken fillets. The presence of O2 in the MAP gaseous mixtures increased the rate of Campylobacter decline on poultry fillets but in general the counts obtained in aerobic versus anaerobic packs were not significantly (P > 0.05)different. CO2 inhibited the growth of TVC, TEC, LAB and Pseudomonas but only at MAP gaseous combinations containing 50e90% CO2 where concentrations of up to 2000 ppm CO2 were recorded in the fillets after 5 days. Under these conditions a shelf-life in excess of 17 days at 2 C was obtained. Although, dissolved O2, at levels of 33 ppm in 80:20% O2:N2 packs after 3 days, reduced Campylobacter, it also favoured the growth of the other microbes on the chicken. The optimum gaseous mixture for achieving the combined objectives of reducing Campylobacter and extending shelf was therefore 40:30:30 CO2:O2:N2, which achieved a shelf-life in excess of 14 days.
| Original language | English |
|---|---|
| Pages (from-to) | 196-203 |
| Journal | Food Microbiology |
| Volume | 44 |
| Publication status | Published (in print/issue) - 2014 |
Bibliographical note
Reference text: Al-Nehlawi, A., Saldo, J., Vega, L.F., Guri, S., 2013. Effect of high carbon dioxide atmospherepacking and soluble gas stabilization pre-treatment on the shelf-life and quality of chicken drumsticks. Meat Sci. 94 (1), 1-8.
Boskou, G., Debevere, J., 1997. Reduction of trimethylamine oxide by Shewanella spp. under modified atmospheres in vitro. Food Microbiol. 14 (6), 543-553.
Boysen, L., Knochel, S., Rosenquist, H., 2007. Survival of Campylobacter jejuni in different gas mixtures. FEMS Microbiol. Lett. 266 (2), 152-157.
Byrd, J.A., Sams, A.R., Hargis, B.M., Caldwell, D.J., 2011. Effect of selected modified atmosphere packing on Campylobacter survival in raw poultry. Poult. Sci. 90 (6), 1324-1328.
Carroll, J.J., Slupsky, J.D., Mather, A.E., 1991. The solubility of carbon dioxide in water at low pressure. J. Phys. Chem. Ref. Data 20 (6), 1201-1209.
Charles, N., Williams, S.K., Rodrick, G.E., 2006. Effects of packaging systems on the
natural microflora and acceptability of chicken breast meat. Poult. Sci. 85 (10), 1798-1801.
Chouliara, E., Karatapanis, A., Savvaidis, I.N., Kontominas, M.G., 2007. Combined effect of oregano essential oil and modified atmosphere packing on shelf-life extension of fresh chicken breast meat, stored at 4�C. Food Microbiol. 24 (6), 607-617.
Devlieghere, F., Debevere, J., 2000. Influence of dissolved carbon dioxide on the growth of spoilage bacteria. Food Sci. Technol. 33 (8), 531-537.
Devlieghere, F., Debevere, J., van Impe, J., 1998. Concentration of carbon dioxide in the water-phase as a parameter to model the effect of a modified atmosphere on microorganisms. Int. J. Food Microbiol. 43 (1e2), 105-113.
European Food Safety Authority (EFSA), 2010. Analysis of the baseline survey on the prevalence of Campylobacter in broiler batches and of Campylobacter and Salmonella on broiler carcasses in the EU, 2008, Part A: Campylobacter and Salmonella prevalence estimates. EFSA J. 2010 (8), 1e100. Available online: www. efsa.europa.eu.
Farber, J.M., 1991. Microbiological aspects of modified-atmosphere packaging technology e a review. J. Food Prot. 54, 58-70.
Fletcher, G.C., Summers, G., Corrigan, V., Cumarasamy, S., Dufour, J.P., 2002. Spoilage of king salmon (Oncorhynchus tshawytscha) fillets stored under different atmospheres. J. Food Sci. 67 (6), 2362-2374.
Fletcher, G.C., Summers, G., Corrigan, V.K., Johanson, M.R., Hedderley, D., 2004. Optimizing gas mixtures for modified atmosphere packaging of fresh king salmon (Oncorhynchus tshawytscha). J. Aquat. Good Prod. Technol. 13 (4), 5-28.
Gill, C.O., 1988. The solubility of carbon dioxide in meat. Meat Sci. 22 (1), 65-71.
Gill, C.O., Harrison, J.C.L., Penney, N., 1990. The storage life of chicken carcasses packaged under carbon-dioxide. Int. J. Food Microbiol. 11 (2), 151-157.
Harvey, P., Leach, S., 1998. Analysis of coccal cell formation by Campylobacter jejuni using continuous culture techniques, and the importance of oxidative stress. J. Appl. Microbiol. 85 (2), 398-404.
Haughton, P.N., Lyng, J.G., Morgan, D.J., Cronin, D.A., Noci, F., Fanning, S., Whyte, P., 2010. An evaluation of the potential of high-intensity ultrasound for improving the microbial safety of poultry. Food Bioprocess Technol. 5 (3), 992-998.
Huat, J.T.Y., Aziz, S.A., Abu, J., Ghazali, F.M., Chilek, T.Z.T., Ahmad, N., Sandra1, A., Nishibuchi, M., Radu, S., 2010. Thermophilic Campylobacter spp. occurrence on chickens at farm, slaughter house and retail. Int. J. Poult. Sci. 9 (2), 134-138.
International Commission on Microbiological Specifications for Foods (ICMSF), 1986. In: Microorganisms in Foods. Sampling for Microbiological Analysis: Principles and Scientific Applications, second ed., vol. 2. University of Toronto Press, Toronto, pp. 181-196.
Jakobsen, M., Bertelsen, G., 2004. Predicting the amount of carbon dioxide absorbed in meat. Meat Sci. 68 (4), 603-610.
Jakobsen, M., Bertelsen, G., 2006. Solubility of carbon dioxide in fat and muscle tissue. J. Muscle Foods 17 (1), 9-19.
Jakobsen, M., Risbo, J., 2009. Carbon dioxide equilibrium between product and gas phase of modified atmosphere packaging systems: exemplified by semi-hard cheese. J. Food Eng. 92 (3), 285-290.
Jay, J.M., 1986. Microbial Spoilage indicators and metabolites. In: Pierson, M.D., Stern, A. (Eds.), Foodborne Microorganisms and Their Toxins. Developing Methodology. Marcel Dekker Inc., Basel, pp. 213-240.
Jimenez, S.M., Salsi, M.S., Tiburzi, M.C., Rafaghelli, R.C., Tessi, M.A., Coutaz, V.R., 1997. Spoilage microflora in fresh chicken breast stored at 4 degrees C: influence of packaging methods. J. Appl. Microbiol. 83, 613-618.
Jones, D.M., Sutcliffe, E.M., Rios, R., Fox, A.J., Curry, A., 1993. Campylobacter jejuni adapts to aerobic metabolism in the environment. J. Med. Microbiol. 38 (2), 145-150.
King, D.A., Nagel, C.W., 1975. Influence of carbon dioxide upon the metabolism of Pseudomonas aeruginosa. J. Food Sci. 40 (2), 362.
Klancnik, A., Bernarda, G., Jamnik, P., Vuckovic, D., Abram, M., Smole Mozina, S., 2009. Stress response and pathogenic potential of Campylobacter jejuni cells exposed to starvation. Res. Microbiol. 160 (5), 345-352.
Nychas, G.-J.E., Skandamis, P.N., Tassou, C.C., Koutsoumanis, K.P., 2008. Meat spoilage during distribution. Meat Sci. 78 (1e2), 77-89.
Patsias, A., Chouliara, I., Paleologos, E.K., Savvaidis, I., Kontominas, M.G., 2006a
Relation of biogenic amines to microbial and sensory changes of precooked chicken meat stored aerobically and under modified atmosphere packaging at 4 degrees C. Eur. Food Res. Technol. 223 (5), 683-689.
Patsias, A., Chouliara, A., Badeka, A., savvaidis, I.N., Kontominas, M.G., 2006b. Shelflife of a chilled precooked chicken product stored in air and under modified atmospheres: microbiological, chemical, sensory attributes. Food Microbiol. 23 (5), 423-429.
Prini, R.F., Crovetto, R., 1989. Evaluation of data on solubility of simple apolar gases in light and heavy water at high temperature. J. Phys. Chem. Ref. Data 18 (3), 1231-1243.
Rajkovic, A., Tomic, N., Smigic, N., Uyttendaele, M., Ragaert, P., Devlieghere, F., 2010. Survival of Campylobacter jejuni on raw chicken legs packed in high-oxygen or high-carbon dioxide atmosphere after the decontamination with lactic acid/ sodium lactate buffer. Int. J. Food Microbiol. 140 (2e3), 201-206.
Ranson, S.L., Walker, D.A., Clarke, I.D., 1960. Effects of carbon dioxide on mitochondrial enzymes from ricinus. Biochemistry 76 (2), 216-221.
Rotabakk, B.T., Lekand, O.I., Sivertsvik, M., 2007. Volumetric method to determine carbon dioxide solubility and absorption rate in foods packaged in flexible or semi rigid package. J. Food Eng. 82 (1), 43-50.
Rotabakk, B.J., Lekang, O.-I., Siverstsvik, M., 2010. Solubility, absorption and desorption of carbon dioxide in chicken breast fillets. Food Sci. Technol. 43 (3), 442-446.
Sade, E., Murros, A., Bjorkroth, J., 2013. Predominant enterobacteria on modified atmosphere
packaged meat and poultry. Food Microbiol. 34 (2), 252-258.
Sears, D.F., Eisenberg, R.M., 1961. A model representing a physiological role of CO2 at the cell membrane. Genet. Eng. Biotechnol. News 44, 869.
Sivertsvik, M., Jensen, J.S., 2005. Solubility and absorption of carbon dioxide into non-respiring foods. Part 3: cooked meat products. J. Food Eng. 70 (4), 499-505.
Sivertsvik, M., Rosnes, J.T., Jeksrud, W.K., 2004. Solubility and absorption rate of carbon dioxide into non-respiring foods. Part 2: raw fish fillets. J. Food Eng. 63 (4), 451-458.
Stiles, M.E., 1991a. Scientific principles of controlled/modified atmosphere packaging. In: Ooraikul, B., Stiles, M.E. (Eds.), Modified Atmosphere Packaging of Food. Ellis Horwood Ltd., Chichester, England, pp. 18e25, 118-147.
Stiles, M.E., 1991b. Modified atmosphere packaging of meat, poultry and their products. In: Ooraikul, B., Stiles, M.E. (Eds.), Modified Atmosphere Packaging of Food. Ellis Horwood Limited, Chichester, England, pp. 118-147.
Storz, G., Imlay, J.A., 1999. Oxidative stress. Curr. Opin. Microbiol. 2, 188-194.
Thippareddi, H., Phebus, R.K., 2007. Modified atmosphere packaging (MAP): microbial control and quality. Pork Inf. Factsheet 12, 1-5.
Wolfe, S.K., 1980. Use of CO2 and CO2 enriched atmospheres for meats, fish and produce. Food Technol. 34 (3), 55-58.
Keywords
- Campylobacter
- Poultry
- Modified atmospheric packaging
- Shelf-life
