A systematic characterization of the distribution, biofilm-forming potential and the resistance of the biofilms to the CIP processes of the bacteria in a milk powder processing factory

Food Research International

Volumn 113, Issue , 2018, Pages 316-326

  Zou, Mingming ^a   Liu, Donghong ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Acid tolerance; Alkali tolerance; Bacillus spp.; Bacterial biofilms; Milk powder processing facility

Indexed keywords

BACTERIA; BACTERIOLOGY; BIOFILMS; DAIRIES; RNA; SODIUM HYDROXIDE;

16S RRNA GENE SEQUENCE; ACID TOLERANCE; BACILLUS SPP; BACTERIAL BIOFILM; EFFECTS OF TEMPERATURE; INCUBATION TEMPERATURES; MILK POWDER; PATHOGENIC MICROORGANISMS;

BIOHAZARDS;

ACID; ALKALI;

ANIMAL; BACTERIUM; BIOFILM; DAIRYING; DRUG EFFECT; FOOD HANDLING; HEAT; MICROBIOLOGY; MILK; PH; POWDER; PROCEDURES; RADIATION RESPONSE;

ACIDS; ALKALIES; ANIMALS; BACTERIA; BIOFILMS; DAIRYING; FOOD HANDLING; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; MILK; POWDERS;

EID: 85050079091     PISSN: 09639969     EISSN: 18737145     Source Type: Journal    
DOI: 10.1016/j.foodres.2018.07.020     Document Type: Article

References (35)

1. Bourne, D.G., Høj, L., Webster, N.S., Swan, J., Hall, M.R., Biofilm development within a larval rearing tank of the tropical rock lobster, Panulirus ornatus. Aquaculture 260:1–4 (2006), 27–38.
2. Burgess, S.A., Lindsay, D., Flint, S.H., Thermophilic bacilli and their importance in dairy processing. International Journal of Food Microbiology 144:2 (2010), 215–225.
3. Cappitelli, F., Polo, A., Villa, F., Biofilm formation in food processing environments is still poorly understood and controlled. Food Engineering Reviews 6:1–2 (2014), 29–42.
4. Carpentier, B., Cerf, O., Biofilms and their consequences, with particular reference to hygiene in the food industry. Journal of Applied Microbiology 75:6 (1993), 499–511.
5. Centola Vidal, A.M., Rossi Junior, O.D., de Abreu, I.L., Buerger, K.P., Cardoso, M.V., Siqueira Goncalves, A.C., D'Abreu, L.F., Detection of Bacillus cereus isolated during ultra high temperature milk production flowchart through random amplified polymorphic DNA polymerase chain reaction. Ciencia Rural 46:2 (2016), 286–292.
6. Cherif-Antar, A., Moussa-Boudjemâa, B., Didouh, N., Medjahdi, K., Mayo, B., Flórez, A.B., Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant. Dairy Science and Technology 96:1 (2016), 1–12.
7. Chmielewski, R.A.N., Frank, J.F., Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety 2:1 (2010), 22–32.
8. Ciccio, P.D., Vergara, A., Festino, A.R., Paludi, D., Zanardi, E., Ghidini, S., Ianieri, A., Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control 50 (2015), 930–936.
9. Donlan, R.M., Costerton, J.W., Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15(2), 2002, 167.
10. Faille, C., Fontaine, F., Bénézech, T., Potential occurrence of adhering living Bacillus spores in milk product processing lines. Journal of Applied Microbiology 90:6 (2001), 892–900.
11. Giaouris, E.D., Nychas, G.J., The adherence of Salmonella Enteritidis PT4 to stainless steel: the importance of the air-liquid interface and nutrient availability. Food Microbiology 23:8 (2006), 747–752.
12. Hamanakaa, D., Genkawa, T., Tanaka, F., Uchino, T., Effects of temperature and nutrient concentration on the structural characteristics and removal of vegetable-associated Pseudomonas biofilm. Food Control 24:1–2 (2012), 165–170.
13. Hill, B.M., Smythe, B.W., Endospores of thermophilic bacteria in ingredient milk powders and their significance to the manufacture of sterilized milk products: An industrial perspective. Food Reviews International 28:3 (2012), 299–312.
14. Hinton, A.R., Trinh, K.T., Brooks, J.D., Manderson, G.J., Thermophile survival in milk fouling and on stainless steel during cleaning. Food and Bioproducts Processing 80:4 (2003), 299–304.
15. Huck, J.R., Woodcock, N.H., Ralyea, R.D., Boor, K.J., Molecular subtyping and characterization of psychrotolerant endospore-forming bacteria in two New York State fluid milk processing systems. Journal of Food Protection 70:10 (2007), 2354–2364.
16. Jessen, B., Lammert, L., Biofilm and disinfection in meat processing plants. International Biodeterioration and Biodegradation 51:4 (2003), 265–269.
17. Klavenes, A., Stalheim, T., Sjøvold, O., Josefsen, K., Granum, P.E., Attachment of Bacillus cereus spores with and without appendages to stainless steel surfaces. Food and Bioproducts Processing 80:4 (2003), 312–318.
18. Kumari, S., Sarkar, P.K., In vitro model study for biofilm formation by Bacillus cereus in dairy chilling tanks and optimization of clean-in-place (CIP) regimes using response surface methodology. Food Control 36:1 (2014), 153–158.
19. Lee, S.H., Barancelli, G.V., Camargo, T.M.D., Corassin, C.H., Rosim, R.E., Cruz, A.G.D., Cappato, L.P., Biofilm-producing ability of Listeria monocytogenes isolates from Brazilian cheese processing plants. Food Research International 91 (2016), 88–91.
20. Lee, S.H., Mangolin, B.L., Goncalves, J.L., Neeff, D.V., Silva, M.P., Cruz, A.G., Oliveira, C.A., Biofilm-producing ability of Staphylococcus aureus isolates from Brazilian dairy farms. Journal of Dairy Science 97:3 (2014), 1812–1816.
21. Lin, Y., Ren, F., Zhao, L., Guo, H., Genotypes and the persistence survival phenotypes of Bacillus cereus isolated from UHT milk processing lines. Food Control 82 (2017), 48–56.
22. Maifreni, M., Frigo, F., Bartolomeoli, I., Buiatti, S., Picon, S., Marino, M., Bacterial biofilm as a possible source of contamination in the microbrewery environment. Food Control 50 (2015), 809–814.
23. Møretrø T., Hermansen, L., Holck, A.L., Sidhu, M.S., Rudi, K., Langsrud, S., Biofilm formation and the presence of the intercellular adhesion locus ica among staphylococci from food and food processing environments. Applied and Environmental Microbiology, 69(9), 2003, 5648.
24. Murphy, P.M., Lynch, D., Kelly, P.M., Growth of thermophilic spore forming bacilli in milk during the manufacture of low heat powders. International Journal of Dairy Technology 52:2 (1999), 45–50.
25. Nam, H.M., Lim, S.K., Kang, H.M., Kim, J.M., Moon, J.S., Jang, K.C., Jung, S.C., Prevalence and antimicrobial susceptibility of gram-negative bacteria isolated from bovine mastitis between 2003 and 2008 in Korea. Journal of Dairy Science 92:5 (2009), 2020–2026.
26. Pillai, S.K., Sakoulas, G., Eliopoulos, G.M., Moellering, R.C., Murray, B.E., Inouye, R.T., Effects of glucose on fsr-mediated biofilm formation in Enterococcus faecalis. Journal of Infectious Diseases 190:5 (2004), 967–970.
27. Rivas, L., Dykes, G.N., A comparative study of biofilm formation by Shiga toxigenic Escherichia coli using epifluorescence microscopy on stainless steel and a microtitre plate method. Journal of Microbiological Methods 69:1 (2007), 44–51.
28. Rossi, C., Serio, A., Chaves-López, C., Anniballi, F., Auricchio, B., Goffredo, E., Paparella, A., Biofilm formation, pigment production and motility in Pseudomonas spp. isolated from the dairy industry. Food Control 86 (2018), 241–248.
29. Sadiq, F.A., Flint, S., Yuan, L., Li, Y., Liu, T., He, G., Propensity for biofilm formation by aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders. International Journal of Food Microbiology 262 (2017), 89–98.
30. Scott, S.A., Brooks, J.D., Rakonjac, J., Walker, K.M.R., Flint, S.H., The formation of thermophilic spores during the manufacture of whole milk powder. International Journal of Dairy Technology 60:2 (2007), 109–117.
31. Sharma, M., Anand, S.K., Biofilms evaluation as an essential component of HACCP for food/dairy processing industry – a case. Food Control 13:6 (2002), 469–477.
32. Stanga, M., Sanitation: cleaning and disinfection in the food industry. Sanitation Cleaning & Disinfection in the Food Industry 126:3 (2010), 239–250.
33. Stepanović S., Vuković D., Dakić I., Savić B., Švabić-Vlahović M., A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods 40:2 (2000), 175–179.
34. Yuan, D.D., Liu, G.C., Ren, D.Y., Zhang, D., Zhao, L., Kan, C.P., Zhang, L.B., A survey on occurrence of thermophilic bacilli in commercial milk powders in China. Food Control 25:2 (2012), 752–757.
35. Zain, S.N.M., Flint, S.H., Bennett, R., Tay, H.-S., Characterisation and biofilm screening of the predominant bacteria isolated from whey protein concentrate 80. Dairy Science & Technology 96:3 (2015), 285–295.