Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-29T12:12:05.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Microbiological quality of raw milk attributable to prolonged refrigeration conditions

Published online by Cambridge University Press:  02 March 2017

Nuwan R Vithanage ,
Muditha Dissanayake ,
Greg Bolge ,
Enzo A Palombo ,
Thomas R Yeager  and
Nivedita Datta
Nuwan R Vithanage
Affiliation:
College of Health and Biomedicine, Victoria University, Werribee, Victoria 3030, Australia Advanced Food Systems Research Unit, Victoria University, Werribee, Victoria 3030, Australia
Muditha Dissanayake
Affiliation:
College of Health and Biomedicine, Victoria University, Werribee, Victoria 3030, Australia Advanced Food Systems Research Unit, Victoria University, Werribee, Victoria 3030, Australia
Greg Bolge
Affiliation:
Murray Goulburn Co-operative Co Ltd, Leongatha, Victoria 3953, Australia
Enzo A Palombo
Affiliation:
Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia
Thomas R Yeager*
Affiliation:
Advanced Food Systems Research Unit, Victoria University, Werribee, Victoria 3030, Australia College of Engineering and Science, Victoria University, Werribee, Victoria 3030, Australia Institute for Sustainability and Innovation, Victoria University, Werribee, Victoria 3030, Australia
Nivedita Datta
Affiliation:
College of Health and Biomedicine, Victoria University, Werribee, Victoria 3030, Australia Institute for Sustainability and Innovation, Victoria University, Werribee, Victoria 3030, Australia
*
*For correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Refrigerated storage of raw milk is a prerequisite in dairy industry. However, temperature abused conditions in the farming and processing environments can significantly affect the microbiological quality of raw milk. Thus, the present study investigated the effect of different refrigeration conditions such as 2, 4, 6, 8, 10 and 12 °C on microbiological quality of raw milk from three different dairy farms with significantly different initial microbial counts. The bacterial counts (BC), protease activity (PA), proteolysis (PL) and microbial diversity in raw milk were determined during storage. The effect of combined heating (75 ± 0·5 °C for 15 s) and refrigeration on controlling those contaminating microorganisms was also investigated. Results of the present study indicated that all of the samples showed increasing BC, PA and PL as a function of temperature, time and initial BC with a significant increase in those criteria ≥6 °C. Similar trends in BC, PA and PL were observed during the extended storage of raw milk at 4 °C. Both PA and PL showed strong correlation with the psychrotrophic proteolytic count (PPrBC: at ≥4 °C) and thermoduric psychrotrophic count (TDPC: at ≥8 °C) compared to total plate count (TPC) and psychrotrophic bacterial count (PBC), that are often used as the industry standard. Significant increases in PA and PL were observed when PPrBC and TDPC reached 5 × 104 cfu/ml and 1 × 104 cfu/ml, and were defined as storage life for quality (SLQ), and storage life for safety (SLS) aspects, respectively. The storage conditions also significantly affected the microbial diversity, where Pseudomonas fluorescens and Bacillus cereus were found to be the most predominant isolates. However, deep cooling (2 °C) and combination of heating and refrigeration (≤4 °C) significantly extended the SLQ and SLs of raw milk.

Keywords

Raw milkpsychrotrophic proteolytic bacteriathermoduric psychrotrophsdiversityprotease activityproteolysis
Type
Research Article
Information
Journal of Dairy Research , Volume 84 , Issue 1 , February 2017 , pp. 92 - 101
Copyright
Copyright © Proprietors of Journal of Dairy Research 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anzueto, ME 2014 Tracking Heat-Resistant, Sporeforming Bacteria in the Milk Chain: a Farm to Table Approach. Master Thesis. Lincoln, Nebraska: University of Nebraska. http://digitalcommons.unl.edu/foodscidiss/45.Google Scholar
Bach, HJ, Hartmann, A, Schloter, M & Munch, JC 2001 PCR primers and functional probes for amplification and detection of bacterial genes for extracellular peptidases in single strains and in soil. Journal of Microbiological Methods 44 173–182 Google Scholar
Buehner, KP, Anand, S & Garcia, A 2014 Prevalence of thermoduric bacteria and spores on 10 Midwest dairy farms. Journal of Dairy Science 97 6777–6784 Google Scholar
Burger, M, Woods, RG, McCarthy, C & Beacham, IR 2000 Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator. Microbiology 146 3149–3155 Google Scholar
Cempírkova, R 2007 Contamination of cow's raw milk by psychrotrophic and mesophilic microflora in relation to selected factors. Czech Journal of Animal Science 52 387–393 Google Scholar
Champagne, CP, Laing, RR, Roy, D, Mafu, AA, Griffiths, MW & White, C 1994 Psychrotrophs in dairy products: their effects and their control. Critical Reviews in Food Science & Nutrition 34 1–30 Google Scholar
Christiansson, A, Naidu, AS, Nilsson, I, Wadström, T & Pettersson, H 1989 Toxin production by Bacillus cereus dairy isolates in milk at low temperatures. Applied Environmental Microbiology 55 2595–2600 Google Scholar
Cousin, MA 1982 Presence and activity of psychrotrophic microorganisms in milk and dairy products: a review. Journal of Food Protection 45 172–207 Google Scholar
Cupp-Enyard, C 2009 Use of the protease fluorescent detection kit to determine protease activity. Journal of Visualized Experiments 30 1514–1521 Google Scholar
Datta, N & Deeth, HC 2003 Diagnosing the cause of proteolysis in UHT milk. LWT – Food Science and Technology 36 173–182 Google Scholar
Dogan, B & Boor, KJ 2003 Genetic diversity and spoilage potentials among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Applied and Environmental Microbiology 69 130–138 Google Scholar
Dufour, D, Nicodème, M, Perrin, C, Driou, A, Brusseaux, E, Humbert, G, Gaillard, J-L & Dary, A 2008 Molecular typing of industrial strains of Pseudomonas spp. isolated from milk and genetical and biochemical characterization of an extracellular protease produced by one of them. International Journal of Food Microbiology 125 188–196 Google Scholar
FSANZ 2012 Raw Milk Temperatures-Understanding the and Complying with EU Requirements. Australia: Department of Agriculture and water resources. http://www.agriculture.gov.au/SiteCollectionDocuments/aqis/exporting/dairy/goods-for-eu/raw-milk-temps.pdf (accessed 18 August 2014)Google Scholar
FSANZ 2014 Understanding and Complying with European Union Requirements for Raw Milk Temperatures, pp. 1–4. Australia: Department of Agiculture and water resources. http://www.foodstandards.gov.au/code/primaryproduction/dairy (accessed 16 August 2014)Google Scholar
Gillis, WT, Cartledge, MF, Rodriguez, IR & Suarez, EJ 1985 Effect of raw milk quality on ultra-high temperature processed milk. Journal of Dairy Science 68 2875–2879 Google Scholar
Griffiths, MW, Phillips, JD & Muir, DD 1987 Effect of low-temperature storage on the bacteriological quality of raw milk. Food Microbiology 4 285–291 CrossRefGoogle Scholar
Hantsis-Zacharov, E & Halpern, M 2007 Culturable psychrotrophic bacterial communities in raw milk and their proteolytic and lipolytic traits. Applied and Environmental Microbiology 73 7162–7168 Google Scholar
Haryani, S, Datta, N, Elliott, AJ & Deeth, HC 2003 Production of proteinases by psychrotrophic bacteria in raw milk stored at low temperature. Australian Journal of Dairy Technology 58 15–20 Google Scholar
Lafarge, V, Ogier, J-C, Girard, V, Maladen, V, Leveau, J-Y, Gruss, A & Delacroix-Buchet, A 2004 Raw cow milk bacterial population shifts attributable to refrigeration. Applied and Environmental Microbiology 70 5644–5650 Google Scholar
Ma, S, Li, H, Yan, C, Wang, D, Li, H, Xia, X, Dong, X, Zhao, Y, Sun, T, Hu, P & Guan, W 2014 Antagonistic effect of protein extracts from Streptococcus sanguinis on pathogenic bacteria and fungi of the oral cavity. Experimental and Therapeutic Medicine 7 1486–1494 Google Scholar
Machado, SG, Bazzolli, DMS & Vanetti, MCD 2013 Development of a PCR method for detecting proteolytic psychrotrophic bacteria in raw milk. International Dairy Journal 29 8–14 CrossRefGoogle Scholar
Marchand, S, Heylen, K, Messens, W, Coudijzer, K, De Vos, P, Dewettinck, K, Herman, L, De Block, J & Heyndrickx, M 2009a Seasonal influence on heat-resistant proteolytic capacity of Pseudomonas lundensis and Pseudomonas fragi, predominant milk spoilers isolated from Belgian raw milk samples. Environmental Microbiology 11 467–482 Google Scholar
Marchand, S, Vandriesche, G, Coorevits, A, Coudijzer, K, De Jonghe, V, Dewettinck, K, De Vos, P, Devreese, B, Heyndrickx, M & De Block, J 2009b Heterogeneity of heat-resistant proteases from milk Pseudomonas species. International Journal of Food Microbiology 133 68–77 Google Scholar
McKellar, RC 1981 Development of off-flavors in ultra-high temperature and pasteurized milk as a function of proteolysis1. Journal of Dairy Science 64 2138–2145 Google Scholar
McKellar, RC 1989 Enzymes of Psychrotrophs in Raw Food. Enzymes of Psychrotrophs in Raw Food, 2nd edition, pp. 3–245 (Section A, Chapt. 1–10). Florida, USA: Taylor & Francis Google Scholar
Morita, Y, Nakamura, T, Hasan, Q, Murakami, Y, Yokoyama, K & Tamiya, E 1997 Cold-active enzymes from cold-adapted bacteria. Journal of the American Oil Chemists’ Society 74 441–444 Google Scholar
Munsch-Alatossava, P, Rita, H & Alatossava, T 2007 A faster and more economical alternative to the standard plate count (SPC) method for microbiological analyses of raw milks. In Communicating Current Research and Educational Topics and Trends in Applied Microbiology, pp. 495–499 (Ed. Méndez-Vilas, A). Badajoz: Formatex Google Scholar
O'Connell, A, Ruegg, PL, Jordan, K, O'Brien, B & Gleeson, D 2016 The effect of storage temperature and duration on the microbial quality of bulk tank milk. Journal of Dairy Science 99 3367–3374 Google Scholar
Oliveira, GBD, Favarin, L, Luchese, RH & McIntosh, D 2015 Psychrotrophic bacteria in milk: how much do we really know? Brazilian Journal of Microbiology 46 313–321 Google Scholar
Quigley, L, O'Sullivan, O, Stanton, C, Beresford, TP, Ross, RP, Fitzgerald, GF & Cotter, PD 2013 The complex microbiota of raw milk. FEMS Microbiology Reviews 37 664–698 Google Scholar
Renner, E 1988 Storage stability and some nutritional aspects of milk powders and ultra high temperature products at high ambient temperatures. Journal of Dairy Research 55 125–142 Google Scholar
Silveira, IA, Carvalho, EP, Teixeira, D & Barrios, BE 1999 Verification of the proteolytic and lipolytic activities of the microbial flora isolated from raw, refrigerated, type B milk. II. Psychrotrophic microorganisms. Rev Latinoam Microbiology 41 85–89 Google Scholar
Slattery, H & Fitzgerald, RJ 1998 Functional properties and bitterness of sodium caseinate hydrolysates prepared with a Bacillus proteinase. Journal of Food Science 63 418–422 Google Scholar
Srairi, MT, Benhouda, H, Kuper, M & Le Gal, PY 2009 Effect of cattle management practices on raw milk quality on farms operating in a two-stage dairy chain. Tropical Animal Health Production 41 259–272 Google Scholar
Stadhouders, J 1982 Cooling and thermization as a means to extend the keeping quality of raw milk. Kieler milchwirtschaftliche Forschungsberichte 34 19–28 Google Scholar
Valik, L, Gorner, F & Laukova, D 2003 Growth dynamics of Bacillus cereus and shelf-life of pasteurised milk. Czech Journal of Food Sciences 21 195–202 Google Scholar
Vine, NG, Leukes, WD & Kaiser, H 2004 In vitro growth characteristics of five candidate aquaculture probiotics and two fish pathogens grown in fish intestinal mucus. FEMS Microbiology Letters 231 145–152 Google Scholar
Vissers, MMM & Driehuis, F 2009 On-farm hygienic milk production. In Milk Processing and Quality Management, pp. 1–22 (Chapt.1) (Ed. Tamime, AY). West Sussex, UK: Wiley-Blackwell Google Scholar
Vithanage, NR, Yeager, TR, Jadhav, SR, Palombo, EA & Datta, N 2014 Comparison of identification systems for psychrotrophic bacteria isolated from raw bovine milk. International Journal of Food Microbiology 189 26–38 Google Scholar
Vithanage, NR, Dissanayake, M, Bolge, G, Palombo, EA, Yeager, TR & Datta, N 2016 Biodiversity of culturable psychrotrophic microbiota in raw milk attributable to refrigeration conditions, seasonality and their spoilage potential. International Dairy Journal 57 80–90 Google Scholar
von Neubeck, M, Baur, C, Krewinkel, M, Stoeckel, M, Kranz, B, Stressler, T, Fischer, L, Hinrichs, J, Scherer, S & Wenning, M 2015 Biodiversity of refrigerated raw milk microbiota and their enzymatic spoilage potential. International Journal of Food Microbiology 211 57–65 Google Scholar
Vyletělová, M & Hanuš, O 2000a Effects of contamination by Pseudomonas fluorescens on principal components and technological parameters of pasteurized milk during storage. Czech Journal of Food Sciences 18 224–234 Google Scholar
Vyletelova, M, Hanus, O, Urbanova, E & Kopunecz, P 2000b The occurrence and identification of psychrotrophic bacteria with proteolytic and lipolytic activity in bulk milk samples at storage in primary production conditions. Czech Journal of Animal Science 45 373–383 Google Scholar
Zarei, M, Ebrahimpour, A, Abdul-Hamid, A, Anwar, F & Saari, N 2012 Production of defatted palm kernel cake protein hydrolysate as a valuable source of natural antioxidants. International Journal of Molecular Sciences 13 8097–8111 Google Scholar
Supplementary material: PDF

Vithanage supplementary material

Tables S1-S3 and Figure S1

Download Vithanage supplementary material(PDF)
PDF 527.9 KB