Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection

Journal of Dairy Science

Volumn 99, Issue 8, 2016, Pages 6105-6120

  Trmcic A ^a   Chauhan, K ^a   Kent, D J ^a   Ralyea, R D ^a   Martin, N H ^a   Boor, K J ^a   Wiedmann, M ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

cheese; coliform; fecal contamination; pasteurization; pathogen

Indexed keywords

WATER;

ANALYSIS; ANIMAL; CHEESE; ENTEROBACTERIACEAE; FECES; FOOD CONTROL; FOOD HANDLING; ISOLATION AND PURIFICATION; LISTERIA MONOCYTOGENES; MICROBIOLOGY; MILK; PASTEURIZATION; PH; PROCEDURES; SALMONELLA; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

ANIMALS; CHEESE; ENTEROBACTERIACEAE; FECES; FOOD HANDLING; FOOD INSPECTION; FOOD MICROBIOLOGY; HYDROGEN-ION CONCENTRATION; LISTERIA MONOCYTOGENES; MILK; PASTEURIZATION; SALMONELLA; SHIGA-TOXIGENIC ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS; WATER;

EID: 84973537738     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2016-11112     Document Type: Article

References (81)

1. Abriouel, H., Martin-Platero, A., Maqueda, M., Valdivia, E., Martinez-Bueno, M., Biodiversity of the microbial community in a Spanish farmhouse cheese as revealed by culture-dependent and culture-independent methods. Int. J. Food Microbiol. 127 (2008), 200–208 http://dx.doi.org/10.1016/j.ijfoodmicro.2008.07.004.
2. Almeida, G., Figueiredo, A., Rola, M., Barros, R.M., Gibbs, P., Hogg, T., Teixeira, P., Microbiological characterization of randomly selected Portuguese raw milk cheeses with reference to food safety. J. Food Prot. 70 (2007), 1710–1716.
3. Almeida, G., Magalhaes, R., Carneiro, L., Santos, I., Silva, J., Ferreira, V., Hogg, T., Teixeira, P., Foci of contamination of Listeria monocytogenes in different cheese processing plants. Int. J. Food Microbiol. 167 (2013), 303–309 http://dx.doi.org/10.1016/j.ijfoodmicro.2013.09.006.
4. Bachmann, H.P., Spahr, U., The fate of potentially pathogenic bacteria in Swiss hard and semihard cheeses made from raw milk. J. Dairy Sci. 78 (1995), 476–483 http://dx.doi.org/10.3168/jds.S0022-0302(95)76657-7.
5. Baylis, C., Uyttendaele, M., Joosten, H., Davies, A., The Enterobacteriaceae and their Significance to the Food Industry. ILSI Europe Report Series, 2011, International Life Sciences Institute, Washington, DC, 1–52.
6. Brady, C., Cleenwerck, I., Venter, S., Coutinho, T., De Vos, P., Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): Proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter. Syst. Appl. Microbiol. 36 (2013), 309–319 http://dx.doi.org/10.1016/j.syapm.2013.03.005.
7. Brady, C., Hunter, G., Kirk, S., Arnold, D., Denman, S., Rahnella victoriana sp. nov., Rahnella bruchi sp. nov., Rahnella woolbedingensis sp. nov., classification of Rahnella genomospecies 2 and 3 as Rahnella variigena sp. nov. and Rahnella inusitata sp. nov., respectively and emended description of the genus Rahnella. Syst. Appl. Microbiol. 37 (2014), 545–552 http://dx.doi.org/10.1016/j.syapm.2014.09.001.
8. Brooks, J.C., Martinez, B., Stratton, J., Bianchini, A., Krokstrom, R., Hutkins, R., Survey of raw milk cheeses for microbiological quality and prevalence of foodborne pathogens. Food Microbiol. 31 (2012), 154–158 http://dx.doi.org/10.1016/j.fm.2012.03.013.
9. Buchanan, R.L., Acquisition of microbiological data to enhance food safety. J. Food Prot. 63 (2000), 832–838.
10. Cabedo, L., Picart i Barrot, L., Teixido i Canelles, A., Prevalence of Listeria monocytogenes and Salmonella in ready-to-eat food in Catalonia, Spain. J. Food Prot. 71 (2008), 855–859.
11. Chaves-López, C., De Angelis, M., Martuscelli, M., Serio, A., Paparella, A., Suzzi, G., Characterization of the Enterobacteriaceae isolated from an artisanal Italian ewe's cheese (Pecorino Abruzzese). J. Appl. Microbiol. 101 (2006), 353–360 http://dx.doi.org/10.1111/j.1365-2672.2006.02941.x.
12. Colak, H., Hampikyan, H., Bingol, E.B., Ulusoy, B., Prevalence of L. monocytogenes and Salmonella spp. in Tulum cheese. Food Contr. 18 (2007), 576–579 http://dx.doi.org/10.1016/j.foodcont.2006.02.004.
13. Cole, J.R., Chai, B., Farris, R.J., Wang, Q., Kulam, S.A., McGarrell, D.M., Garrity, G.M., Tiedje, J.M., The Ribosomal Database Project (RDP-II): Sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 33 (2005), D294–D296 http://dx.doi.org/10.1093/nar/gki038.
14. Correll, W.A., Letter to American Cheese Society (ACS) with an Update on What Has Been Done with Respect to Non-toxigenic Escherichia coli (E. coli) in Raw Milk Cheese, 2014, Public Health Service, Food and Drug Administration, College Park, MD.
15. Coton, M., Delbés-Paus, C., Irlinger, F., Desmasures, N., Le Fleche, A., Stahl, V., Montel, M.-C., Coton, E., Diversity and assessment of potential risk factors of gram-negative isolates associated with French cheeses. Food Microbiol. 29 (2012), 88–98 http://dx.doi.org/10.1016/j.fm.2011.08.020.
16. Coveney, H.M., Fitzgerald, G.F., Daly, C., A study of the microbiological status of Irish farmhouse cheeses with emphasis on selected pathogenic and spoilage microorganisms. J. Appl. Bacteriol. 77 (1994), 621–630 http://dx.doi.org/10.1111/j.1365-2672.1994.tb02810.x.
17. D'Amico, D.J., Donnelly, C.W., Microbiological quality of raw milk used for small-scale artisan cheese production in Vermont: Effect of farm characteristics and practices. J. Dairy Sci. 93 (2010), 134–147 http://dx.doi.org/10.3168/jds.2009-2426.
18. D'Amico, D.J., Groves, E., Donnelly, C.W., Low incidence of foodborne pathogens of concern in raw milk utilized for farmstead cheese production. J. Food Prot. 71 (2008), 1580–1589.
19. Dalmasso, M., Jordan, K., Process environment sampling can help to reduce the occurrence of Listeria monocytogenes in food processing facilities. Ir. J. Agric. Food Res. 52 (2012), 93–100.
20. Davidson, P.M., Roth, L.A., Gambrel-Lenarz, S.A., Coliform and other indicator bacteria. Wehr, H.M., Frank, J.F., (eds.) Standard Methods for the Examination of Dairy Products, 17th, 2004, American Public Health Association, Washington, DC, 187–226.
21. Delbès-Paus, C., Pochet, S., Helinck, S., Veisseire, P., Bord, C., Lebecque, A., Coton, M., Desmasures, N., Coton, E., Irlinger, F., Montel, M.-C., Impact of gram-negative bacteria in interaction with a complex microbial consortium on biogenic amine content and sensory characteristics of an uncooked pressed cheese. Food Microbiol. 30 (2012), 74–82 http://dx.doi.org/10.1016/j.fm.2011.12.008.
22. Delcenserie, V., Taminiau, B., Delhalle, L., Nezer, C., Doyen, P., Crevecoeur, S., Roussey, D., Korsak, N., Daube, G., Microbiota characterization of a Belgian protected designation of origin cheese, Herve cheese, using metagenomic analysis. J. Dairy Sci. 97 (2014), 6046–6056 http://dx.doi.org/10.3168/jds.2014-8225.
23. Dugan, K.A., Lawrence, H.S., Hares, D.R., Fisher, C.L., Budowle, B., An improved method for post-PCR purification for mtDNA sequence analysis. J. Forensic Sci. 47 (2002), 811–818.
24. Dugat-Bony, E., Straub, C., Teissandier, A., Onesime, D., Loux, V., Monnet, C., Irlinger, F., Landaud, S., Leclercq-Perlat, M.N., Bento, P., Fraud, S., Gibrat, J.F., Aubert, J., Fer, F., Guedon, E., Pons, N., Kennedy, S., Beckerich, J.M., Swennen, D., Bonnarme, P., Overview of a surface-ripened cheese community functioning by meta-omics analyses. PLoS One, 10, 2015, e0124360 http://dx.doi.org/10.1371/journal.pone.0124360.
25. Edberg, S.C., Rice, E.W., Karlin, R.J., Allen, M.J., Escherichia coli: The best biological drinking water indicator for public health protection. Symp. Ser. Soc. Appl. Microbiol. 29 (2000), 106S–116S.
26. Esho, F.K., Enkhtuya, B., Kusumoto, A., Kawamoto, K., Microbial assessment and prevalence of foodborne pathogens in natural cheeses in Japan. Biomed Res. Int., 2013, 2013, 205801 http://dx.doi.org/10.1155/2013/205801.
27. Feng, P., S. D. Weagant, and K. Jinneman. 2011. Diarrheagenic Escherichia coli. Chapter 4A in Bacteriological Analytical Manual (BAM). http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm070080.htm.
28. Feresu, S., Nyati, H., Fate of pathogenic and non-pathogenic Escherichia coli strains in two fermented milk products. J. Appl. Bacteriol. 69 (1990), 814–821.
29. Filiousis, G., Johansson, A., Frey, J., Perreten, V., Prevalence, genetic diversity and antimicrobial susceptibility of Listeria monocytogenes isolated from open-air food markets in Greece. Food Contr. 20 (2009), 314–317 http://dx.doi.org/10.1016/j.foodcont.2008.05.018.
30. Gaulin, C., Ramsay, D., Bekal, S., Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. J. Food Prot. 75 (2012), 71–78 http://dx.doi.org/10.4315/0362-028X.JFP-11-236.
31. Gill, A., Oudit, D., Enumeration of Escherichia coli O157 in outbreak-associated Gouda cheese made with raw milk. J. Food Prot. 78 (2015), 1733–1737 http://dx.doi.org/10.4315/0362-028X.JFP-15-036.
32. Hitchins, A. D., and K. Jinneman. 2013. Detection and enumeration of Listeria monocytogenes in foods. Chapter 10 in Bacteriological Analytical Manual (BAM). Accessed Feb. 13, 2014. http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm071400.htm.
33. Ho, A.J., Lappi, V.R., Wiedmann, M., Longitudinal monitoring of Listeria monocytogenes contamination patterns in a farmstead dairy processing facility. J. Dairy Sci. 90 (2007), 2517–2524 http://dx.doi.org/10.3168/jds.2006-392.
34. Hu, Y., Zhang, Q., Meitzler, J.C., Rapid and sensitive detection of Escherichia coli O157:H7 in bovine faeces by a multiplex PCR. J. Appl. Microbiol. 87 (1999), 867–876.
35. Huck, J.R., Sonnen, M., Boor, K.J., Tracking heat-resistant, cold-thriving fluid milk spoilage bacteria from farm to packaged product. J. Dairy Sci. 91 (2008), 1218–1228 http://dx.doi.org/10.3168/jds.2007-0697.
36. Irlinger, F., Yung, S.A., Sarthou, A.-S., Delbès-Paus, C., Montel, M.-C., Coton, E., Coton, M., Helinck, S., Ecological and aromatic impact of two Gram-negative bacteria (Psychrobacter celer and Hafnia alvei) inoculated as part of the whole microbial community of an experimental smear soft cheese. Int. J. Food Microbiol. 153:3 (2012), 332–338 a, http://dx.doi.org/10.1016/j.ijfoodmicro.2011.11.022.
37. Irlinger, F., Layec, S., Helinck, S., Dugat-Bony, E., Cheese rind microbial communities: Diversity, composition and origin. FEMS Microbiol. Lett. 362 (2015), 1–11 http://dx.doi.org/10.1093/femsle/fnu015.
38. Irlinger, F., Loux, V., Bento, P., Gibrat, J.F., Straub, C., Bonnarme, P., Landaud, S., Monnet, C., Genome sequence of Staphylococcus equorum ssp. equorum Mu2, isolated from a French smear-ripened cheese. J. Bacteriol. 194 (2012), 5141–5142 b, http://dx.doi.org/10.1128/JB.01038-12.
39. Jackson, E.E., Erten, E.S., Maddi, N., Graham, T.E., Larkin, J.W., Blodgett, R.J., Schlesser, J.E., Reddy, R.M., Detection and enumeration of four foodborne pathogens in raw commingled silo milk in the United States. J. Food Prot. 75 (2012), 1382–1393 http://dx.doi.org/10.4315/0362-028X.JFP-11-548.
40. Jayarao, B.M., Wang, L., A study on the prevalence of gram-negative bacteria in bulk tank milk. J. Dairy Sci. 82 (1999), 2620–2624 http://dx.doi.org/10.3168/jds.S0022-0302(99)75518-9.
41. Kornacki, J.L., Indicator organism assays: Chaos, confusion and criteria. Food Safety Mag. 17 (2011), 26–28.
42. Kousta, M., Mataragas, M., Skandamis, P., Drosinos, E.H., Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food Contr. 21 (2010), 805–815 http://dx.doi.org/10.1016/j.foodcont.2009.11.015.
43. Leclerc, H., Mossel, D.A., Edberg, S.C., Struijk, C.B., Advances in the bacteriology of the coliform group: Their suitability as markers of microbial water safety. Annu. Rev. Microbiol. 55 (2001), 201–234 http://dx.doi.org/10.1146/annurev.micro.55.1.201.
44. Little, C.L., Rhoades, J.R., Sagoo, S.K., Harris, J., Greenwood, M., Mithani, V., Grant, K., McLauchlin, J., Microbiological quality of retail cheeses made from raw, thermized or pasteurized milk in the UK. Food Microbiol. 25 (2008), 304–312 http://dx.doi.org/10.1016/j.fm.2007.10.007.
45. Loncarevic, S., Danielsson-Tham, M.L., Tham, W., Occurrence of Listeria monocytogenes in soft and semi-soft cheeses in retail outlets in Sweden. Int. J. Food Microbiol. 26 (1995), 245–250.
46. Luo, C., Walk, S.T., Gordon, D.M., Feldgarden, M., Tiedje, J.M., Konstantinidis, K.T., Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc. Natl. Acad. Sci. USA 108 (2011), 7200–7205 http://dx.doi.org/10.1073/pnas.1015622108.
47. Manfreda, G., De Cesare, A., Stella, S., Cozzi, M., Cantoni, C., Occurrence and ribotypes of Listeria monocytogenes in Gorgonzola cheeses. Int. J. Food Microbiol. 102 (2005), 287–293 http://dx.doi.org/10.1016/j.ijfoodmicro.2004.11.045.
48. Manolopoulou, E., Sarantinopoulos, P., Zoidou, E., Aktypis, A., Moschopoulou, E., Kandarakis, I.G., Anifantakis, E.M., Evolution of microbial populations during traditional Feta cheese manufacture and ripening. Int. J. Food Microbiol. 82 (2003), 153–161.
49. Martin, N.H., Ranieri, M.L., Murphy, S.C., Ralyea, R.D., Wiedmann, M., Boor, K.J., Results from raw milk microbiological tests do not predict the shelf-life performance of commercially pasteurized fluid milk. J. Dairy Sci. 94 (2011), 1211–1222 http://dx.doi.org/10.3168/jds.2010-3915.
50. Masiello, S.N., Martin, N.H., Trmčić, A., Wiedmann, M., Boor, K.J., Identification and characterization of psychrotolerant coliform bacteria isolated from pasteurized fluid milk. J. Dairy Sci. 99 (2016), 130–140 http://dx.doi.org/10.3168/jds.2015-9728.
51. Mena, C., Almeida, G., Carneiro, L., Teixeira, P., Hogg, T., Gibbs, P.A., Incidence of Listeria monocytogenes in different food products commercialized in Portugal. Food Microbiol. 21 (2004), 213–216 http://dx.doi.org/10.1016/S0740-0020(03)00057-1.
52. Morales, P., Fernandez-Garcia, E., Nunez, M., Caseinolysis in cheese by Enterobacteriaceae strains of dairy origin. Lett. Appl. Microbiol. 37 (2003), 410–414.
53. Mossel, D.A.A., Corry, J.E.L., Struijk, C.B., Baird, R.M., (eds.) Essentials of the Microbiology of Foods. A Textbook for Advanced Studies, 1995, J. Wiley, Chichester, UK.
54. Mullan, W.M.A., Causes and control of early gas production in cheddar cheese. Int. J. Dairy Technol. 53 (2000), 63–68 http://dx.doi.org/10.1111/j.1471-0307.2000.tb02660.x.
55. Nightingale, K., Bovell, L., Grajczyk, A., Wiedmann, M., Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotyping. J. Microbiol. Methods 68 (2007), 52–59 http://dx.doi.org/10.1016/j.mimet.2006.06.005.
56. Oberg, E.N., Oberg, C.J., Motawee, M.M., Martini, S., McMahon, D.J., Increasing stringiness of low-fat mozzarella string cheese using polysaccharides. J. Dairy Sci. 98 (2015), 4243–4254 http://dx.doi.org/10.3168/jds.2014-8733.
57. Oh, S., Buddenborg, S., Yoder-Himes, D.R., Tiedje, J.M., Konstantinidis, K.T., Genomic diversity of Escherichia isolates from diverse habitats. PLoS One, 7, 2012, e47005 http://dx.doi.org/10.1371/journal.pone.0047005.
58. Pantoja, J.C., Reinemann, D.J., Ruegg, P.L., Associations among milk quality indicators in raw bulk milk. J. Dairy Sci. 92 (2009), 4978–4987 http://dx.doi.org/10.3168/jds.2009-2329.
59. Paruch, A.M., Maehlum, T., Specific features of Escherichia coli that distinguish it from coliform and thermotolerant coliform bacteria and define it as the most accurate indicator of faecal contamination in the environment. Ecol. Indic. 23 (2012), 140–142 http://dx.doi.org/10.1016/j.ecolind.2012.03.026.
60. Pintado, C.M.B.S., Oliveira, A., Pampulha, M.E., Ferreira, M.A.S.S., Prevalence and characterization of Listeria monocytogenes isolated from soft cheese. Food Microbiol. 22 (2005), 79–85 http://dx.doi.org/10.1016/j.fm.2004.04.004.
61. Qi, W., Lacher, D.W., Bumbaugh, A.C., Hyma, K.E., Ouellette, L.M., Large, T.M., Tarr, C.L., Whittam, T.S., EcMLST: An online database for multi locus sequence typing of pathogenic Escherichia coli. Proc. 2004 IEEE Computational Systems Bioinformatics Conference (CSB 2004), 2004, IEEE Computer Society, Stanford, CA, 520–521.
62. Quigley, L., O'Sullivan, O., Stanton, C., Beresford, T.P., Ross, R.P., Fitzgerald, G.F., Cotter, P.D., The complex microbiota of raw milk. FEMS Microbiol. Rev. 37 (2013), 664–698 http://dx.doi.org/10.1111/1574-6976.12030.
63. Quinto, E.J., Cepeda, A., Incidence of toxigenic Escherichia coli in soft cheese made with raw or pasteurized milk. Lett. Appl. Microbiol. 24 (1997), 291–295 http://dx.doi.org/10.1046/j.1472-765X.1997.00072.x.
64. Reginald, W. B., and G. A. Lancette. 2001. Staphylococcus aureus. Chapter 12 in Bacteriological Analytical Manual (BAM). Accessed Feb. 13, 2014. http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm071429.htm.
65. Rosengren, Å., Fabricius, A., Guss, B., Sylvén, S., Lindqvist, R., Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm-dairies. Int. J. Food Microbiol. 144 (2010), 263–269 http://dx.doi.org/10.1016/j.ijfoodmicro.2010.10.004.
66. Rudol, M., Scherer, S., High incidence of Listeria monocytogenes in European red smear cheese. Int. J. Food Microbiol. 63 (2001), 91–98 http://dx.doi.org/10.1016/S0168-1605(00)00413-X.
67. Sauders, B.D., Overdevest, J., Fortes, E., Windham, K., Schukken, Y., Lembo, A., Wiedmann, M., Diversity of Listeria species in urban and natural environments. Appl. Environ. Microbiol. 78 (2012), 4420–4433 http://dx.doi.org/10.1128/AEM.00282-12.
68. Schoder, D., Skandamis, P., Wagner, M., Assessing in-house monitoring efficiency by tracing contamination rates in cheese lots recalled during an outbreak of listeriosis in Austria. Int. J. Food Microbiol. 167 (2013), 353–358 http://dx.doi.org/10.1016/j.ijfoodmicro.2013.09.020.
69. Schvartzman, M.S., Gonzalez-Barron, U., Butler, F., Jordan, K., Modeling the growth of Listeria monocytogenes on the surface of smear- or mold-ripened cheese. Front. Cell. Infect. Microbiol., 4, 2014, 90 http://dx.doi.org/10.3389/fcimb.2014.00090.
70. Sheehan, J.J., Cheese: Avoidance of gas blowing. Fuquay, J.W., Fox, P.F., McSweeney, P.L.H., (eds.) Encyclopedia of Dairy Sciences, 2nd, 2011, Academic Press, San Diego, CA, 661–666.
71. Stevens, M., Ashbolt, N., Cunliffe, D., Review of Coliforms as Microbial Indicators of Drinking Water Quality. Recommendations to Change the Use of Coliforms as Microbial Indicators of Drinking Water Quality, 2003, Australian Government, National Health and Medical Research Council. Biotext Pty Ltd., Canberra, Australia.
72. Strongin, D. 2015. Some things matter. Cheese report. Accessed Jan. 20, 2016. http://www.cheesereporter.com/Strongin/strongin.november6.2015.htm.
73. Tham, W.A., Hajdu, L.J., Danielsson-Tham, M.L., Bacteriological quality of on-farm manufactured goat cheese. Epidemiol. Infect. 104 (1990), 87–100.
74. Trancoso-Reyes, N., Gutierrez-Mendez, N., Sepulveda, D.R., Hernandez-Ochoa, L.R., Assessing the yield, microstructure, and texture properties of miniature Chihuahua-type cheese manufactured with a phospholipase A1 and exopolysaccharide-producing bacteria. J. Dairy Sci. 97 (2014), 598–608 http://dx.doi.org/10.3168/jds.2013-6624.
75. Trmčić, A., Martin, N.H., Boor, K.J., Wiedmann, M., A standard bacterial isolate set for research on contemporary dairy spoilage. J. Dairy Sci. 98 (2015), 5806–5817 http://dx.doi.org/10.3168/jds.2015-9490.
76. US FDA, Center for Food Safety and Applied Nutrition. 2010. Guidance for FDA Staff: Compliance Policy Guide Sec. 527.300 Dairy Products—Microbial Contaminates and Alkaline Phosphatase Activity. Accessed Dec. 10, 2014. http://www.fda.gov/downloads/ICECI/ComplianceManuals/CompliancePolicyGuidanceManual/UCM238465.pdf.
77. Walk, S.T., Alm, E.W., Gordon, D.M., Ram, J.L., Toranzos, G.A., Tiedje, J.M., Whittam, T.S., Cryptic lineages of the genus Escherichia. Appl. Environ. Microbiol. 75 (2009), 6534–6544 http://dx.doi.org/10.1128/AEM.01262-09.
78. Wallace, H. A., A. Jacobson, and T. Hammack. 2012. Salmonella. Chapter 10 in Bacteriological Analytical Manual (BAM). Accessed Feb. 13, 2014. http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm070149.htm.
79. Wolfe, B.E., Button, J.E., Santarelli, M., Dutton, R.J., Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158 (2014), 422–433 http://dx.doi.org/10.1016/j.cell.2014.05.041.
80. Wu, J., Long, S.C., Das, D., Dorner, S.M., Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J. Water Health 9 (2011), 265–278. http://dx.doi.org/10.2166/wh.2011.117.
81. Wu, Q., Tun, H.M., Leung, F.C., Shah, N.P., Genomic insights into high exopolysaccharide-producing dairy starter bacterium Streptococcus thermophilus ASCC 1275. Sci. Rep., 4, 2014, 4974 http://dx.doi.org/10.1038/srep04974.