This study evaluates the influence of inadequate transport conditions on the microbiological quality of chilled chicken meat packaged in plain and modified atmosphere packaging (MAP). The experiments simulated the temperature increase during sample transport to 8, 11, 14, 17, 20, and 25°C with exposure times of 1, 2, 3, and 4 h. Aerobic plate count (APC), psychrotrophic microorganisms count (PMC), β-D-glucuronidase-positive Escherichia coli, and Salmonella spp. were evaluated immediately after the exposure to the elevated temperature (0 h), 3 h, and 24 h after the return to the temperature of ≤4°C. The upper acceptable limits for APC and PMC were set for each combination of investigated chicken meat and packaging type, taking also the initial bacterial condition into account. Chilled chicken breast samples in plain packaging exceeded the APC limits in 16 cases and PMC limits in 20 cases when exposed to temperatures of >4°C, while only 2 MAP samples exceeded APC limits and 8 samples PMC limits, respectively. In chicken legs, 8 samples in plain packaging exceeded the APC limits and 15 the PMC limits, while 12 samples in MAP exceeded the APC limits and 19 the PMC limits. In 402 samples (31.9%) in which the presence of E. coli was detected, its amount ranged from 1.70 to 3.65 log CFU.g-1. It was more commonly detected in chicken legs (255 of 630; 40.5%) than chicken breasts (147 of 630; 23.3%) but was not related to exposure temperature, exposure time, or time until examination. The presence of Salmonella spp. was not detected in any of the samples. Data acquired in the presented study will be used in the development of software helping the national supervisory authorities in the Czech Republic to evaluate whether inadequate transport of samples to analytical laboratories could have affected the microbiological profile of the sample.

Department of Animal Origin Food and Gastronomic Sciences Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno 61242 Brno Czech Republic

Department of Food Hygiene and Safety Faculty of Biotechnology and Food Sciences Slovak University of Agriculture in Nitra 94976 Nitra Slovak Republic

RECETOX Faculty of Science Masaryk University 62500 Brno Czech Republic; Institute of Biostatistics and Analyses Faculty of Medicine Masaryk University 62500 Brno Czech Republic

Zobrazit více v PubMed

Bartáková K., Bursová Š., Necidová L., Haruštiaková D., Zouharová A., Vorlová L., Klimešová M. The effect of cold chain disruption on the microbiological profile of chilled fish. J. Microbiol. Bioltechnol. Food Sci. 2023;13:e9883.

Bailey M., Taylor R., Brar J., Corkran S., Velásquez C., Novoa-Rama E., Oliver H.F., Singh M. Prevalence and antimicrobial resistance of Salmonella from antibiotic-free broilers during organic and conventional processing. J. Food Protect. 2020;83:491–496. PubMed

Belucco S., Barco L., Roccato A., Ricci A. Escherichia coli and Enterobacteriaceae counts on poultry carcasses along the slaughterline: A systematic review and meta-analysi. Food Contr. 2016;60:269–280.

Bruckner S., Albrecht A., Petersen B., Kreyenschmidt J. Influence of cold chain interruptions on the shelf life of fresh pork and poultry. Int. J. Food Sci. Technol. 2012;47:1639–1646.

Bruckner S., Albrecht A., Petersen B., Kreyenschmidt J. A predictive shelf life model as a tool for the improvement of quality management in pork and poultry chains. Food Contr. 2013;29:451–460.

Casaburi A., Piombino P., Nychas G.-J., Villani F., Ercolini D. Bacterial populations and the volatilome associated to meat spoilage. Food Microbiol. 2015;45:83–102. PubMed

Cauchie E., Delhalle L., Taminiau B., Tahiri A., Korsak N., Burteau S., Fall P.A., Farnir F., Baré G., Daube G. Assessment of spoilage bacterial communities in food wrap and modified atmospheres-packed minced pork meat samples by 16S rDNA metagenetic analysis. Front. Microbiol. 2020;10:3074. PubMed PMC

ČSN EN ISO 4833-1 . Metrology and Testing; Prague, Czech Republic: 2014. Food chain microbiology—horizontal method for determining the number of microorganisms—part 1: Tentering technique and calculating colonies cultivated at 30°C. Czech Office for standards.

ČSN EN ISO 6579-1 . Metrology and Testing; Prague, Czech Republic: 2020. Microbiology of the food chain —horizontal method for the detection, enumeration and serotyping of Salmonella—part 1: Detection of Salmonella spp. Czech Office for standards.

ČSN EN ISO 6887-1 . Metrology and Testing; Prague, Czech Republic: 2018. Microbiology of the food chain—preparation of test samples, initial suspension and decimal dilutions for microbiological examination—part 1: General rules for the preparation of the initial suspension and decimal dilutions. Czech Office for standards.

ČSN ISO 16649-2 . Metrology and Testing; Prague, Czech Republic: 2003. Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of b-glucuronidase-positive Escherichia coli—part 2: Colony-count technique at 44°C using 5-bromo-4-chloro-3-indolyl b-D-glucuronide. Czech Office for standards.

ČSN ISO 17410 . Metrology and Testing; Prague, Czech Republic: 2020. Microbiology of the food chain—horizontal method for the enumeration of psychrotrophic microorganisms. Czech Office for standards.

ČSN 569609 . Metrology and Testing; Prague, Czech Republic: 2008. Guides to good hygiene and manufacturing practices – Microbiological criteria for foods. Principles for the establishment and application. Czech Office for Standards.

Da Silva N.B., Longhi D.A., Martins W.F., de Aragãoa G.M.F., Carciofi B.A.M. Mathematical modeling of Lactobacillus viridescens growth in vacuum packed sliced ham under non isothermal conditions. Procedia Food Sci. 2016;7:33–36. PubMed

Demirhan B., Candogan K. Active packing of chicken meats with modified atmosphere including oxygen scavengers. Poult. Sci. 2017;96:1394–1401. PubMed

EFSA/ECDC The European Union One Health 2022 Zoonoses Report. EFSA J. 2023;21:e8442. PubMed PMC

European Union Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Offic. J. Europ. Union, L 139: 55-205.

European Union Regulation (EU) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Offic. J. Europ. Union, L 338: 1-26.

European Union Regulation (EC) No 1333/2008 of the European Parliament and of the Council of 16 December 2008 on food additives. Offic. J. Europ. Union, L 354: 16-33.

Ghollasi-Mood F., Mohsenzadeh M., Hoseindokht M.R., Varidi M. Quality changes of air-packaged chicken meat stored under different temperature conditions and mathematical modelling for predicting the microbial growth and shelf life. J. Food Saf. 2016;37:1–9.

Hansen A.Å., Langsrud S., Carlehog M., Haugen J.E.&., Moen B. CO2 packing increases shelf life through reduction of off-odor production by Cag tolerant bacteria in addition to growth inhibition of the spoilage bacteria. Food Contr. 2023;144

Hauge S.J., Bjørkøy S., Holthe J., Røtterud O., Skjerve E., Midtsian M., Lian I., Alvseike O.&., Nagel-Alne GE. Assesment of in-plant decontamination of broiler carcasses by immersion in hot water and lactic acid in Norway. Food Contr. 2023;152

Hauge S.J., Johannessen G.S., Haverkamp T.H.A., Bjørkøy S., Llarena A.K., Spilsberg B., Leithaug M., Økland M., Holthe J., Røtterud O., Alvseike O.&., Nagel-Alne GE. Assesment of poultry proces hygiene and bacterial dynamics along two broiler slaughter lines in Norway. Food Contr. 2023;146

Herbert U., Albrecht A., Kreyenschmidt J. Definition of predictor variables for MAP poultry filets stored under different temperature conditions. Poult. Sci. 2015;94:424–432. PubMed

Lee K.Y., Lavelle K., Huang A., Atwill E.R., Pitesky M.&., Li X. Assessment of prevalence and diversity of antimicrobial resistant Escherichia coli from retail meats in Southern California. Antibiotics. 2023;12:782. PubMed PMC

Leistner L. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 2000;55:181–186. PubMed

Rouger A., Moriceau N., Prévost H., Remenant B., Zagorec M. Diversity of bacterial communities in French chicken cuts stored under modified atmosphere packaging. Food Microbiol. 2018;70:7–16. PubMed

Soro A.B., Whyte P., Bolton D.J., Tiwari BK. Strategies and novel technologies to control Campylobacter in the poultry chain: A review. Comprehens. Rev. Food Sci. Food Saf. 2020;19:1353–1577. PubMed

Suchánek M., Plzák Z., Šubrt P., Koruna I. Kvalimetrie 7. Validace analytických metod. Eurachem-ČR, PrahaRheumatol. 1997;137:137.

Svobodová I., Bořilová G., Hulánková R., Steinhauserová I. Microbiological quality of broiler carcasses during slaughter processing. Acta Vet. Brno. 2012;81:37–42.

Teles P.F.S., Boiago M.M., Frigo A., Rampazzo L., Araújo D.N., Kich J.D., Rebelatto R., Furian T.Q.&., Stefani LM. Genetic similarities of Escherichia coli isolated from different substrates of the broiler production chain. Braz. J. Poult. Sci. 2021;23:1–6.

Tuncer B., Sireli UT. Microbial growth on broiler carcasses stored at different temperatures after air- or water-chilling. Poult. Sci. 2008;87:793–799. PubMed

Yimenu S.M., Koo J., Kim B.S., Kim J.H.&., Kim JY. Freshness-based real-time shelf-life estimation of packaged chicken meat tunder dynamic storage conditions. Poult. Sci. 2019;98:6921–6930. PubMed PMC

Zouharová A., Bartáková K., Bursová Š., Necidová L., Haruštiaková D., Klimešová M., Vorlová L. Packaging of meat and fish and its impact on the shelf life—a review. Acta Vet. Brno. 2023;92:63–76.