Spoilage of microfiltered and pasteurized extended shelf life milk is mainly induced by psychrotolerant spore-forming bacteria that often originate from recontamination

Frontiers in Microbiology

Volumn 8, Issue JAN, 2017, Pages

  Doll, Etienne V ^a   Scherer, Siegfried ^a   Wenning, Mareike ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Extended shelf life (ESL) milk; Microbiota; Microfiltration; Psychrotolerant spore forming bacteria; Spoilage

Indexed keywords

ACTINOBACTERIA; BACILLUS CEREUS; BACTERIAL SPORE; BIODIVERSITY; DISINFECTION; MICROFILTRATION; MICROFLORA; MILK; NONHUMAN; PAENIBACILLUS; PREVALENCE; SANITATION; SHELF LIFE; SPECIES;

EID: 85011961547     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00135     Document Type: Article

References (55)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
2. Bartoszewicz, M., Hansen, B. M., and Swiecicka, I. (2008). The members of the Bacillus cereus group are commonly present contaminants of fresh and heat-treated milk. Food Microbiol. 25, 588-596. doi: 10.1016/j.fm.2008.02.001
3. Caplan, Z., and Barbano, D. M. (2013). Shelf life of pasteurized microfiltered milk containing 2% fat1. J. Dairy Sci. 96, 8035-8046. doi: 10.3168/jds.2013-6657
4. Chawla, R., Patil, G. R., and Singh, A. K. (2011). High hydrostatic pressure technology in dairy processing: a review. J. Food Sci. Technol. 48, 260-268. doi: 10.1007/s13197-010-0180-4
5. Coorevits, A., De Jonghe, V., Vandroemme, J., Reekmans, R., Heyrman, J., Messens, W., et al. (2008). Comparative analysis of the diversity of aerobic spore-forming bacteria in raw milk from organic and conventional dairy farms. Syst. Appl. Microbiol. 31, 126-140. doi: 10.1016/j.syapm.2008.03.002
6. Datta, N., and Deeth, H. (1999). High pressure processing of milk and dairy products. Aust. J. Dairy Technol. 54, 41-48.
7. Drancourt, M., Roux, V., Fournier, P.-E., and Raoult, D. (2004). rpoB gene sequence-based identification of aerobic Gram-positive cocci of the genera Streptococcus, Enterococcus, Gemella, Abiotrophia, and Granulicatella. J. Clin. Microbiol. 42, 497-504. doi: 10.1128/JCM.42.2.497-504.2004
8. Durak, M. Z., Fromm, H. I., Huck, J. R., Zadoks, R. N., and Boor, K. J. (2006). Development of molecular typing methods for Bacillus spp. and Paenibacillus spp. isolated from fluid milk products. J. Food Sci. 71, M50-M56. doi: 10.1111/j.1365-2621.2006.tb08907.x
9. Elwell, M., and Barbano, D. (2006). Use of Microfiltration to Improve Fluid Milk Quality. J. Dairy Sci. 89, E20-E30. doi: 10.3168/jds. S0022-0302(06)72361-X
10. Eneroth, Å., Svensson, B., Molin, G., and Christiansson, A. (2001). Contamination of pasteurized milk by Bacillus cereus in the filling machine. J. Dairy Res. 68, 189-196. doi: 10.1017/S002202990100485X
11. Faille, C., Fontaine, F., and Bénézech, T. (2001). Potential occurrence of adhering living Bacillus spores in milk product processing lines. J. Appl. Microbiol. 90, 892-900. doi: 10.1046/j.1365-2672.2001.01321.x
12. Fernandez Garcia, L., Alvarez Blanco, S., and Riera Rodriguez, F. A. (2013). Microfiltration applied to dairy streams: removal of bacteria. J. Sci. Food Agric. 93, 187-196. doi: 10.1002/jsfa.5935
13. Fernández García, L., and Riera Rodríguez, F. A. (2014). Combination of microfiltration and heat treatment for ESL milk production: impact on shelf life. J. Food Eng. 128, 1-9. doi: 10.1016/j.jfoodeng.2013.11.021
14. Fricker, M., Skanseng, B., Rudi, K., Stessl, B., and Ehling-Schulz, M. (2011). Shift from farm to dairy tank milk microbiota revealed by a polyphasic approach is independent from geographical origin. Int. J. Food Microbiol. 145(Suppl. 1), S24-S30. doi: 10.1016/j.ijfoodmicro.2010.08.025
15. Fromm, H. I., and Boor, K. (2004). Characterization of pasteurized fluid milk shelf-life attributes. J. Food Sci. 69, M207-M214. doi: 10.1111/j.1365-2621.2004.tb09889.x
16. Hantsis-Zacharov, E., and Halpern, M. (2007). Culturable psychrotrophic bacterial communities in raw milk and their proteolytic and lipolytic traits. Appl. Environ. Microbiol. 73, 7162-7168. doi: 10.1128/AEM.00866-07
17. Harrigan, W. F., and McCance, M. E. (1979). Laboratory Methods in Food and Dairy Microbiology. Metodos de Laboratorio en Microbiologia de Alimentos y Productos Lacteos. London: Academic Press.
18. Holm, S., Malmberg, R., and Svensson, K. (1989). Method for producing milk with a lowered bacterial content. WO86/01687.
19. Huck, J. R., Hammond, B. H., Murphy, S. C., Woodcock, N. H., and Boor, K. J. (2007). Tracking spore-forming bacterial contaminants in fluid milk-processing systems. J. Dairy Sci. 90, 4872-4883. doi: 10.3168/jds.2007-0196
20. Huck, J. R., Sonnen, M., and Boor, K. J. (2008). Tracking heat-resistant, cold-thriving fluid milk spoilage bacteria from farm to packaged product. J. Dairy Sci. 91, 1218-1228. doi: 10.3168/jds.2007-0697
21. Ivy, R. A., Ranieri, M. L., Martin, N. H., Den Bakker, H. C., Xavier, B. M., Wiedmann, M., et al. (2012). Identification and characterization of psychrotolerant sporeformers associated with fluid milk production and processing. Appl. Environ. Microbiol. 78, 1853-1864. doi: 10.1128/AEM.06536-11
22. Kim, M., Oh, H.-S., Park, S.-C., and Chun, J. (2014). Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64, 346-351. doi: 10.1099/ijs.0.059774-0
23. Kim, O.-S., Cho, Y.-J., Lee, K., Yoon, S.-H., Kim, M., Na, H., et al. (2012). Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62, 716-721. doi: 10.1099/ijs.0.038075-0
24. Kumari, S., and Sarkar, P. K. (2016). Bacillus cereus hazard and control in industrial dairy processing environment. Food Control 69, 20-29. doi: 10.1016/j.foodcont.2016.04.012
25. Magnusson, M., Christiansson, A., and Svensson, B. (2007). Bacillus cereus spores during housing of dairy cows: factors affecting contamination of raw milk. J. Dairy Sci. 90, 2745-2754. doi: 10.3168/jds.2006-754
26. Masiello, S. N., Martin, N. H., Watters, R. D., Galton, D. M., Schukken, Y. H., Wiedmann, M., et al. (2014). Identification of dairy farm management practices associated with the presence of psychrotolerant sporeformers in bulk tank milk1. J. Dairy Sci. 97, 4083-4096. doi: 10.3168/jds.2014-7938
27. Mayr, R., Eppert, I., and Scherer, S. (1999). Incidence and identification of psychrotrophic (7 degrees C-tolerant) Bacillus spp. in German HTST pasteurized milk. Milchwissenschaft 54, 26-30.
28. McGuiggan, J., Mccleery, D. R., Hannan, A., and Gilmour, A. (2002). Aerobic spore-forming bacteria in bulk raw milk: factors influencing the numbers of psychrotrophic, mesophilic and thermophilic Bacillus spores. Int. J. Dairy Technol. 55, 100-107. doi: 10.1046/j.1471-0307.2002.00051.x
29. McKinnon, C. H., and Pettipher, G. L. (1983). A survey of sources of heat-resistant bacteria in milk with particular reference to psychrotrophic spore-forming bacteria. J. Dairy Res. 50, 163-170. doi: 10.1017/S0022029900022962
30. Meer, R., Baker, J., Bodyfelt, F., and Griffiths, M. (1991). Psychrotrophic Bacillus spp. in fluid milk products: a review. J. Food Prot. 54, 969-979. doi: 10.4315/0362-028X-54.12.969
31. Nilsson, J., Svensson, B., Ekelund, K., and Christiansson, A. (1998). A RAPD-PCR method for large-scale typing of Bacillus cereus. Lett. Appl. Microbiol. 27, 168-172. doi: 10.1046/j.1472-765X.1998.00402.x
32. Oberreuter, H., Seiler, H., and Scherer, S. (2002). Identification of coryneform bacteria and related taxa by Fourier-transform infrared (FT-IR) spectroscopy. Int. J. Syst. Evol. Microbiol. 52, 91-100. doi: 10.1099/00207713-52-1-91
33. Quigley, L., Mccarthy, R., O'sullivan, O., Beresford, T. P., Fitzgerald, G. F., Ross, R. P., et al. (2013). The microbial content of raw and pasteurized cow milk as determined by molecular approaches. J. Dairy Sci. 96, 4928-4937. doi: 10.3168/jds.2013-6688
34. Ranieri, M. L., Ivy, R. A., Mitchell, W. R., Call, E., Masiello, S. N., Wiedmann, M., et al. (2012). Real-time PCR detection of Paenibacillus spp. in raw milk to predict shelf life performance of pasteurized fluid milk products. Appl. Environ. Microbiol. 78, 5855-5863. doi: 10.1128/AEM.01361-12
35. Salustiano, V., Andrade, N., Soares, N., Lima, J., Bernardes, P., Luiz, L., et al. (2009). Contamination of milk with Bacillus cereus by post-pasteurization surface exposure as evaluated by automated ribotyping. Food Control 20, 439-442. doi: 10.1016/j.foodcont.2008.07.004
36. Schmidt, V. S., Kaufmann, V., Kulozik, U., Scherer, S., and Wenning, M. (2012). Microbial biodiversity, quality and shelf life of microfiltered and pasteurized extended shelf life (ESL) milk from Germany, Austria and Switzerland. Int. J. Food Microbiol. 154, 1-9. doi: 10.1016/j.ijfoodmicro.2011.12.002
37. Shaheen, R., Svensson, B., Andersson, M. A., Christiansson, A., and Salkinoja-Salonen, M. (2010). Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks. Food Microbiol. 27, 347-355. doi: 10.1016/j.fm.2009.11.004
38. Sutherland, A., and Murdoch, R. (1994). Seasonal occurrence of psychrotrophic Bacillus species in raw milk, and studies on the interactions with mesophilic Bacillus sp. Int. J. Food Microbiol. 21, 279-292. doi: 10.1016/0168-1605(94)90058-2
39. Svensson, B., Ekelund, K., Ogura, H., and Christiansson, A. (2004). Characterisation of Bacillus cereus isolated from milk silo tanks at eight different dairy plants. Int. Dairy J. 14, 17-27. doi: 10.1016/j.fm.2009.11.004
40. Svensson, B., Eneroth, Å., Brendehaug, J., and Christiansson, A. (1999). Investigation of Bacillus cereus contamination sites in a dairy plant with RAPD-PCR. Int. Dairy J. 9, 903-912. doi: 10.1016/S0958-6946(00)00014-5
41. Svensson, B., Eneroth, Å., Brendehaug, J., Molin, G., and Christiansson, A. (2000). Involvement of a pasteurizer in the contamination of milk by Bacillus cereus in a commercial dairy plant. J. Dairy Res. 67, 455-460. doi: 10.1017/S0022029900004313
42. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
43. Te Giffel, M., Beumer, R., Langeveld, L., and Rombouts, F. (1997). The role of heat exchangers in the contamination of milk with Bacillus cereus in dairy processing plants. Int. J. Dairy Technol. 50, 43-47. doi: 10.1111/j.1471-0307.1997.tb01734.x
44. te Giffel, M., Van Asselt, A., and De Jong, P. (2006). Shelf extension. Dairy Ind. Int. 71, 44-49.
45. Te Giffel, M., and Van Der Horst, H. (2004). Comparison between bactofugation and microfiltration regarding efficiency of somatic cell and bacteria removal. Bull. Int. Dairy Fed. 389, 49-53.
46. Te Giffel, M. T., Wagendorp, A., Herrewegh, A., and Driehuis, F. (2002). Bacterial spores in silage and raw milk. Antonie Van Leeuwenhoek 81, 625-630. doi: 10.1023/A:1020578110353
47. Tomasula, P. M., Mukhopadhyay, S., Datta, N., Porto-Fett, A., Call, J. E., Luchansky, J. B., et al. (2011). Pilot-scale crossflow-microfiltration and pasteurization to remove spores of Bacillus anthracis (Sterne) from milk. J. Dairy Sci. 94, 4277-4291. doi: 10.3168/jds.2010-3879
48. Trouvé, E., Maubois, J., Piot, M., Madec, M., Fauquant, J., Rouault, A., et al. (1991). Rétention de différentes espèces microbiennes lors de l'épuration du lait par microfiltration en flux tangentiel. Le Lait 71, 1-13. doi: 10.1051/lait:199111
49. Vissers, M. M., Te Giffel, M. C., Driehuis, F., De Jong, P., and Lankveld, J. M. (2007). Minimizing the level of Bacillus cereus spores in farm tank milk. J. Dairy Sci. 90, 3286-3293. doi: 10.3168/jds.2006-873
50. Vithanage, N. R., Dissanayake, M., Bolge, G., Palombo, E. A., Yeager, T. R., and Datta, N. (2016). Biodiversity of culturable psychrotrophic microbiota in raw milk attributable to refrigeration conditions, seasonality and their spoilage potential. Int. Dairy J. 57, 80-90. doi: 10.1016/j.idairyj.2016.02.042
51. von Neubeck, M., Baur, C., Krewinkel, M., Stoeckel, M., Kranz, B., Stressler, T., et al. (2015). Biodiversity of refrigerated raw milk microbiota and their enzymatic spoilage potential. Int. J. Food Microbiol. 211, 57-65. doi: 10.1016/j.ijfoodmicro.2015.07.001
52. Walkling-Ribeiro, M., Rodríguez-González, O., Jayaram, S., and Griffiths, M. W. (2011). Microbial inactivation and shelf life comparison of 'cold' hurdle processing with pulsed electric fields and microfiltration, and conventional thermal pasteurisation in skim milk. Int. J. Food Microbiol. 144, 379-386. doi: 10.1016/j.ijfoodmicro.2010.10.023
53. Wenning, M., Breitenwieser, F., Konrad, R., Huber, I., Busch, U., and Scherer, S. (2014). Identification and differentiation of food-related bacteria: a comparison of FTIR spectroscopy and MALDI-TOF mass spectrometry. J. Microbiol. Methods 103, 44-52. doi: 10.1016/j.mimet.2014.05.011
54. Wenning, M., and Scherer, S. (2013). Identification of microorganisms by FTIR spectroscopy: perspectives and limitations of the method. Appl. Microbiol. Biotechnol. 97, 7111-7120. doi: 10.1007/s00253-013-5087-3
55. Woodburn, M. A., Yousten, A. A., and Hilu, K. H. (1995). Random amplified polymorphic DNA fingerprinting of mosquito-pathogenic and nonpathogenic strains of Bacillus sphaericus. Int. J. Syst. Evol. Microbiol. 45, 212-217.