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Effect of modified atmosphere packaging on physicochemical and microbiological characteristics of Graviera Agraphon cheese during refrigerated storage

Published online by Cambridge University Press:  14 November 2019

Nikolaos Solomakos ,
Maria Govari ,
Evropi Botsoglou  and
Andreana Pexara
Nikolaos Solomakos
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, Karditsa43100, Greece
Maria Govari
Affiliation:
Laboratory of Milk Hygiene and Technology, School of Veterinary Medicine, Aristotle University, Thessaloniki54124, Greece
Evropi Botsoglou
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, Karditsa43100, Greece
Andreana Pexara*
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, Karditsa43100, Greece
*
Author for correspondence: Andreana Pexara, Email: apexara@vet.uth.gr
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Abstract

The aim of this work was to examine the effect of modified atmosphere packaging on the physicochemical and microbiological changes of Graviera Agraphon cheese during refrigerated storage. Blocks of Graviera Agraphon cheese weighing around 200 g were packaged under natural (control) or modified atmosphere packaging (MAP) conditions (50% N2 – 50% CO2) and stored at 4 °C or 10 °C for up to 85 d. Prior to packaging, groups of cheese blocks were inoculated with one each of the following foodborne pathogens at around 104 log cfu/g: Listeria monocytogenes, Salmonella Typhimurium, Escherichia coli O157:H7 or Staphylococcus aureus, whilst further groups of cheese blocks were not inoculated. The protein, fat, moisture and salt contents as well as the pH of control and MAP cheese samples did not change significantly (P > 0.05) throughout 4 °C storage, while the pH values of control and MAP cheese samples were significantly (P < 0.05) reduced at 10 °C storage. At 10 °C storage, yeasts and molds, psychrotrophs and lactic acid bacteria (LAB) were significantly higher (P < 0.05) for the normal atmosphere than the MAP cheese samples after the 4th, 8th and 4th days, respectively. At 4 °C storage, the yeasts and molds or psychrotrophs were significantly higher (P < 0.05) than those of control after the 6th and 15th days, respectively at 4 °C storage. All foodborne pathogens showed a higher decrease (P < 0.05) at 10 °C than 4 °C storage. S. aureus proved more sensitive in inactivation in the MAP conditions than atmospheric conditions. L. monocytogenes and S. aureus presented a higher decrease than that of E. coli O157:H7 and S. Typhimurium. In conclusion, MAP proved efficient in retarding the growth of yeasts, molds, psychrotrophs and E. coli O157:H7, L. monocytogenes, S. Typhimurium and S. aureus in Graviera Agraphon cheese during refrigerated storage at 4 and 10 °C.

Keywords

Graviera Agraphon cheesefood-borne pathogensMAPyeasts and moldsrefrigerated storage
Type
Research Article
Information
Journal of Dairy Research , Volume 86 , Issue 4 , November 2019 , pp. 483 - 489
Copyright
Copyright © Hannah Dairy Research Foundation 2019

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References

Alam, T and Goyal, GK (2011) Effect of MAP on microbiological quality of Mozzarella cheese stored in different packages at 7 ± 1 °C. Journal of Food Science and Technology l48, 120–123.CrossRefGoogle Scholar
Alves, RMV, De Luca Sarantopoulos, CIG, Van Dender, AGF and Faria, JAF (1996) Stability of sliced Mozzarella cheese in modified-atmosphere packaging. Journal of Food Protection 59, 838–844.CrossRefGoogle ScholarPubMed
APHA (2004) In Wehr, HM and Frank, JF (eds), Standard Methods for the Examination of Dairy Products, 17th Edn. Washington, DC: American Public Health Association, p. 570.CrossRefGoogle Scholar
Chen, JH and Hotchkiss, JH (1991) Effect of dissolved carbon dioxide on the growth of psychrotrophic organisms in cottage cheese. Journal of Dairy Science 34, 2941–2945.CrossRefGoogle Scholar
Dermiki, M, Ntzimani, A, Badeka, A, Savvaidis, I and Kontominas, MG 2008 Shelf-life and quality attributes of the whey cheese ‘Myzithra Kalathaki’ using modified atmosphere packaging. LWT-Food Science and Technology 41, 284–294.CrossRefGoogle Scholar
EFSA (2008) The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. EFSA Journal 22, 31–310.Google Scholar
Eklund, T and Jarmund, T (1983) Microculture model studies on the effect of various gas atmospheres on microbial growth at different temperatures. Journal of Applied Bacteriology 55, 119–125.CrossRefGoogle ScholarPubMed
Eliot, SC, Vuillemard, JC and Emond, JP (1998) Stability of shredded mozzarella cheese under modified atmospheres. Journal of Food Science 63, 1075–1080.CrossRefGoogle Scholar
Espie, E, Vaillant, V, Mariani-Kurkdjian, P, Grimont, F, Martin Schaller, R, De Valk, H and Vernozy-Rozand, C (2006) Escherichia coli O157 outbreak associated with fresh unpasteurized goats’ cheese. Epidemiology and Infection 134, 143–146.CrossRefGoogle ScholarPubMed
Farrokh, C, Jordan, K, Auvray, F, Cerf, O, Glass, K, Oppegaard, H, Raynaud, S, Thevenot, D, Condron, R, De Reu, K, Govaris, A, Heggum, K, Heyndrickx, M, Hummerjohann, J, Lindsay, D, Miszczycha, S, Moussiegt, S and Verstraete, K (2013) Review of Shiga-toxin-producing Escherichia coli (STEC) and their significance in dairy production. International Journal of Food Microbiology 162, 190–212.CrossRefGoogle ScholarPubMed
Fletouris, D, Govari, M and Botsoglou, E (2015) The influence of retail display storage on the fatty acid composition of modified atmosphere packaged GravieraAgraphon cheese. International Journal of Dairy Technology 68, 218–226.CrossRefGoogle Scholar
Gammariello, D, Conte, A, Di Giulio, S, Attanasio, M and Nobile, MA (2009) Shelf life of Stracciatella cheese under modified-atmosphere packaging. Journal of Dairy Science 92, 483–490.CrossRefGoogle ScholarPubMed
Giannou, E, Kakouri, A, Matijasic, BB, Rogelj, I and Samelis, J (2009) Fate of Listeria monocytogenes on fully ripened Greek Graviera cheese stored at 4, 12, or 25 °C in air or vacuum packages: In situ PCR detection of a cocktail of bacteriocins potentially contributing to pathogen inhibition. Journal of Food Protection 73, 531–538.CrossRefGoogle Scholar
Gonzalez-Fandos, E, Sanz, S and Olarte, C (2000) Microbiological, physicochemical and sensory characteristics of Cameros cheese packaged under modified atmospheres. Food Microbiology 17, 407–414.CrossRefGoogle Scholar
Govaris, A, Koidis, P and Papatheodorou, K (2002) Survival of Escherichia coli O157:H7 in Feta cheese during storage. Journal of the Hellenic Veterinary Medical Society 53, 24–32.CrossRefGoogle Scholar
Govaris, A, Botsoglou, E, Sergelidis, D and Chatzopoulou, PS (2011) Antibacterial activity of oregano and thyme essential oils against Listeria monocytogenes and Escherichia coli O157:H7 in feta cheese packaged under modified atmosphere. LWT-Food Science and Technology 44, 1240–1244.CrossRefGoogle Scholar
Greek Codex Alimentarius (2003) Official Journal of the Republic of Greece, vol. B, Article 83. Athens: National Printing Office.Google Scholar
ISO 6611:2004 (IDF 94:2004) Preview Milk and milk products – Enumeration of colony-forming units of yeasts and/or moulds – Colony-count technique at 25 °C.Google Scholar
ISO (International Organization for Standardization) (1999) ISO 6888-1: Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of coagulase positive staphylococci (Staphylococcus aureus and other species). International Organization for Standardization, Geneva.Google Scholar
Jelastopulu, E, Venieri, D, Komninou, G, Kolokotronis, T, Constantinidis, TC and Bantias, C (2006) Outbreak of acute gastroenteritis in an air force base in Western Greece. BMC Public Health 6, 254–261.CrossRefGoogle Scholar
Kimura, B, Yoshiyama, T and Fujii, T (1999) Carbon dioxide inhibition of Escherichia coli and Staphylococcus aureus on a pH-adjusted surface in a model system. Journal of Food Science 64, 367–370.CrossRefGoogle Scholar
Kirkin, C, Gunes, G and Kilic-Akyilmaz, M (2013) Preservation of precut white cheese by modified atmosphere packaging. International Journal of Dairy Technology 66, 576–586.Google Scholar
Leistner, L and Gorris, LGM (1995) Food preservation by hurdle technology. Trends in Food Science & Technology 6, 41–46.CrossRefGoogle Scholar
Mexis, SF, Chouliara, E and Kontominas, MG (2011) Quality evaluation of grated Graviera cheese stored at 4 and 12 °C using active and modified atmosphere packaging. Packaging Technology and Science 24, 15–29.CrossRefGoogle Scholar
Millette, M, Luquet, FM and Lacroix, M (2007) In vitro growth control of selected pathogens by Lactobacillus acidophilus and Lactobacillus casei fermented milk. Letters in Applied Microbiology 44, 314–319.CrossRefGoogle ScholarPubMed
Moatsou, G, Moschopoulou, E and Anifantakis, E (2004) Effect of different manufacturing parameters on the characteristics of Graviera Kritis cheese. International Journal of Dairy Technology 57, 215–220.CrossRefGoogle Scholar
Pexara, A, Solomakos, N and Govaris, A (2013) Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in milk and dairy products. Journal of the Hellenic Veterinary Medical Society 64, 17–34.Google Scholar
Pintado, CMBS, Grant, KA, Halford-Maw, R, Hampton, MD, Ferreira, MASS and McLauchlin, J (2009) Association between a case study of asymptomatic ovine listerial mastitis and the contamination of soft cheese and cheese processing environment with Listeria monocytogenes in Portugal. Foodborne Pathogens and Disease 6, 569–575.CrossRefGoogle ScholarPubMed
Samelis, J, Kakouri, A, Pappa, EC, Matijasić, BB, Georgalaki, MD, Tsakalidou, E and Rogelj, A (2010) Microbial stability and safety of traditional Greek Graviera cheese: characterization of the lactic acid bacterial flora and culture-independent detection of bacteriocin genes in the ripened cheeses and their microbial consortia. Journal of Food Protection 73, 1294–1303.CrossRefGoogle ScholarPubMed
Sara, H, Cody, MD, Sharon, L, Abbott, MS, Anthony, A, Marfin, MDMPH, Beth Schulz, MPH, Wagner, P, Robbins, K, Janet, C, Mohle-Boetani, MD, Duc, J and Vugia, MD (1999) Two outbreaks of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Northern California. Journal of the American Medical Association 281, 1805–1810.Google Scholar
Shrestha, S, Grieder, JA, McMahon, DJ and Nummer, BA (2011 a) Survival of Salmonella serovars introduced as a post-aging contaminant during storage of low-salt cheddar cheese at 4, 10, and 21 °C. Journal of Food Science 76, 617–621.CrossRefGoogle ScholarPubMed
Shrestha, S, Grieder, JA, McMahon, DJ and Nummer, BA (2011 b) Survival of Listeria monocytogenes introduced as a post-aging contaminant during storage of low-salt cheddar cheese at 4, 10, and 21 °C. Journal of Dairy Science 94, 4329–4335.CrossRefGoogle ScholarPubMed
Sims, GR, Glenister, DA, Brocklehurst, TF and Lund, BM (1989) Survival and growth of food poisoning bacteria following inoculation into cottage cheese varieties. International Journal of Food Microbiology 9, 173–195.CrossRefGoogle ScholarPubMed
Singh, F, Wani, AA, Karim, AA and Langowski, HC (2012) The use of carbon dioxide in the processing and packaging of milk and dairy products: a review. International Journal of Dairy Technology 65, 161–177.CrossRefGoogle Scholar
Trobetas, A, Badeka, A and Kontominas, MG (2008) Light-induced changes in grated Graviera hard cheese packaged under modified atmospheres. International Dairy Journal 181, 133–1139.Google Scholar
Van Duynhoven, YTHP, Isken, LD, Borgen, K, Besselse, M, Soethoudt, K, Haitsma, O, Mulder, B, Notermans, DW, Jonge, RD, Kock, P, Van Pelt, W, Stenvers, O and Van Steenbergen, J (2009) A prolonged outbreak of Salmonella Typhimurium infection related to an uncommon vehicle: hard cheese made from raw milk. Epidemiology & Infection 137, 1548–1557.CrossRefGoogle Scholar
Whitley, E, Muir, D and Waites, WM (2000) The growth of Listeria monocytogenes in cheese packed under a modified atmosphere. Journal of Applied Microbiology 8, 852–857.Google Scholar