The evolving role of coliforms as indicators of unhygienic processing conditions in dairy foods

Frontiers in Microbiology

Volumn 7, Issue SEP, 2016, Pages

  Martin, Nicole H ^a   Trmcic, Aljoša ^a   Hsieh, Tsung Han ^a   Boor, Kathryn J ^a   Wiedmann, Martin ^a  

^a Cornell University ^*  (United States)

Author keywords

Coliform; Dairy foods; Indicator organisms; Pathogens; Pseudomonas

Indexed keywords

CHEESE; COLIFORM BACTERIUM; DAIRY PRODUCT; ENVIRONMENTAL IMPACT; FECAL COLIFORM; FECES MICROFLORA; FERMENTED MILK PRODUCT; GRAM NEGATIVE BACTERIUM; HEALTH HAZARD; HUMAN; HYGIENE; LACTIC ACID BACTERIUM; MICROBIAL CONTAMINATION; MICROBIOLOGICAL PARAMETERS; MICROORGANISM DETECTION; MILK; NONHUMAN; PASTEURIZATION; RAOULTELLA; REFRIGERATION; REVIEW; TEMPERATURE;

EID: 84993990217     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01549     Document Type: Review

References (61)

1. Abbott, S. L., Cheung, W. K. W., and Janda, J. M. (2003). The genus aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J. Clin. Microbiol. 41, 2348-2357. doi: 10.1128/JCM.41.6.2348-2357.2003
2. Birollo, G. A., Reinheimer, J. A., and Vinderola, C. G. (2001). Enterococci vs non-lactic acid microflora as hygiene indicators for sweetened yoghurt. Food Microbiol. 18, 597-604. doi: 10.1006/fmic.2001.0435
3. Boor, K. J., Brown, D. P., Murphy, S. C., Kozlowski, S. M., and Bandler, D. K. (1998). Microbiological and chemical quality of raw milk in New York State. J. Dairy Sci. 81, 1743-1748. doi: 10.3168/jds.S0022-0302(98)75742-X
4. Brooks, J. C., Martinez, B., Stratton, J., Bianchini, A., Krokstrom, R., and Hutkins, R. (2012). Survey of raw milk cheeses for microbiological quality and prevalence of foodborne pathogens. Food Microbiol. 31, 154-158. doi: 10.1016/j.fm.2012.03.013
5. Busta, F. F., Suslow, T. V., Parish, M. E., Beuchat, L. R., Farber, J. N., Garrett, E. H., et al. (2006). The use of indicators and surrogate microorganisms for the evaluation of pathogens in fresh and fresh-cut produce. Compreh. Rev. Food Sci. Food Saf. 2, 179-185. doi: 10.1111/j.1541-4337.2003.tb00035.x
6. California Department of Food and Agriculture [CDFA] (2016). California Milk Standards, Bacteriological Standards. Available at: https://www.cdfa.ca.gov/ahfss/Milk_and_Dairy_Food_Safety/Milk_Standards.html [accessed July 15, 2016].
7. California Food and Agriculture Code (2016). FOOD AND AGRICULTURAL CODE SECTION 35891-35893. Available at: http://www.leginfo.ca.gov/cgi-bin/displaycode?section=fac&group=35001-36000&file=35891-35893 [accessed July 13, 2016].
8. Carey, N. R., Murphy, S. C., Zadoks, R. N., and Boor, K. J. (2005). Shelf lives of pasteurized fluid milk products in New York State: a ten-year study. Food Prot. Trends 25, 102-113.
9. Chapin, T. K., Nightingale, K. K., Worobo, R. W., Wiedmann, M., and Strawn, L. K. (2014). Geographical and meteorological factors associated with isolation of Listeria species in New York State produce production and natural environments. J. Food. Prot. 77, 1919-1928. doi: 10.4315/0362-028X.JFP-14-132
10. Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M., et al. (1987). Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41, 435-464. doi: 10.1146/annurev.mi.41.100187.002251
11. D'Amico, D. J., Groves, E., and Donnelly, C. W. (2008). Low incidence of foodborne pathogens of concern in raw milk utilized for farmstead cheese production. J. Food Prot. 71, 1580-1589.
12. Dancer, S. J., Shears, P., and Platt, D. J. (1997). Isolation and characterization of coliforms from glacial ice and water in Canada's High Arctic. J. Appl. Microbiol. 82, 597-609. doi: 10.1111/j.1365-2672.1997.tb03590.x
13. Davidson, P. M., Roth, L. A., and Gambrel-Lenarz, S. A. (2004). "Coliform and other indicator bacteria, " in Standard Methods for the Examination of Dairy Products, 17th Edn, eds H. M. Wehr and J. F. Frank (Washington, DC: American Public Health Association), 187-227.
14. Deetae, P., Mounier, J., Bonnarme, P., Spinnler, H. E., Irlinger, F., and Helinck, S. (2009). Effects of Proteus vulgaris growth on the establishment of a cheese microbial community and on the production of volatile aroma compounds in a model cheese. J. Appl. Microbiol. 107, 1404-1413. doi: 10.1111/j.1365-2672.2009.04315.x
15. de Jong, P. (1997). Impact and control of fouling in milk processing. Trends Food Sci. Technol. 8, 401-405. doi: 10.1016/S0924-2244(97)01089-3
16. Duncan, S. E., Yaun, B. R., and Sumner, S. S. (2004). "Microbiological methods for dairy products, " in Standard Methods for the Examination of Dairy Products, 17th Edn, eds H. M. Wehr and J. F. Frank (Washington, DC: American Public Health Association), 249-268.
17. Ehart, B. (2011). NASDA Releases Raw Milk Survey. Washington, DC: The National Association of State Departments of Agriculture (NASDA).
18. El-Sharef, N., Ghenghesh, K. S., Abognah, Y. S., Gnan, S. O., and Rahouma, A. (2006). Bacteriological quality of ice cream in Tripoli-Libya. Food Control 17, 637-641. doi: 10.1016/j.foodcont.2005.04.001
19. European Communities Regulation (2010). European communities regulation commission regulation on microbiological criteria for foodstuffs. Commission regulation (EC) No 365/2010. Off. J. Eur. Union 107, 9-11.
20. Farkye, N. Y. (2000). "Microbiology of cheese making and maturation, " in Encyclopedia of Food Microbiology, Vol. 1, eds R. K. Robinson, C. A. Batt, and P. D. Patel (London: Academic Press), 381-387.
21. FDA (2015). "Standards for grade "A" milk and milk products, " in Grade "A" Pasteurized Milk Ordinance, (Washington, DC: U.S. Department of Health and Human Services, Public Health Service), 28-31.
22. Frank, J. F., and Yousef, A. E. (2004). "Tests for groups of microorganisms, " in Standard Methods for the Examination of Dairy Products, 17th Edn, ed. M. Wehr (Washington, DC: American Public Health Association), 227-248.
23. Hervert, C. J. (2016). The Use of Coliforms, Enterobacteriaceae, and Gram-negative Organisms as Microbial Hygiene Indicators in the Dairy Industry, Master's thesis. Cornell University, Ithaca, NY.
24. Hervert, C. J., Alles, A. S., Martin, N. H., Boor, K. J., and Wiedmann, M. (2016). Evaluation of different methods to detect microbial hygiene indicators relevant in the dairy industry. J. Dairy Sci. 99, 1-10. doi: 10.3168/jds.2016-11074
25. Hogan, J., and Smith, K. L. (2003). Coliform mastitis. Vet. Res. 34, 507-519. doi: 10.1051/vetres:2003022
26. Hughes, K. A. (2003). Aerial dispersal and survival of sewage-derived faecal coliforms in Antarctica. Atmos. Environ. 37, 3147-3155. doi: 10.1016/S1352-2310(03)00207-3
27. Jackson, E. E., Erten, E. S., Maddi, N., Graham, T. E., Larkin, J. W., Blodgett, R. J., et al. (2012). Detection and enumeration of four foodborne pathogens in raw commingled silo milk in the United States. J. Food Prot. 75, 1382-1393. doi: 10.4315/0362-028X.JFP-11-548
28. Jayarao, B. M., and Wang, L. (1999). A study on the prevalence of gram-negative bacteria in bulk tank milk. J. Dairy Sci. 82, 2620-2624. doi: 10.3168/jds.S0022-0302(99)75518-9
29. Johnson, J. (1996). "Predictive microorganisms as an indication of pathogen contamination, " in Proceedings 49th Annual Reciprocal Meat Conference, Vol. 49, Madison, WI, 138-143.
30. Kagkli, D. M., Vancanneyt, M., Vandamme, P., Hill, C., and Cogan, T. M. (2007). Contamination of milk by enterococci and coliforms from bovine faeces. J. Appl. Microbiol. 103, 1393-1405. doi: 10.1111/j.1365-2672.2007.03338.x
31. Khayat, F. A., Bruhn, J. C., and Richardson, G. H. (1988). A survey of coliforms and Staphylococcus aureus in cheese using impedimetric and plate count methods. J. Food Prot. 51, 53-55.
32. Kilb, B., Lange, B., Schaule, G., Flemming, H. C., and Wingender, J. (2003). Contamination of drinking water by coliforms from biofilms grown on rubber-coated valves. Int. J. Hygiene Environ. Health 206, 563-573. doi: 10.1078/1438-4639-00258
33. Kumar, C. G., and Anand, S. K. (1998). Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42, 9-27. doi: 10.1016/S0168-1605(98)00060-9
34. Leclerc, H., Mossel, D. A., Edberg, S. C., and Struijk, C. B. (2001). Advances in the bacteriology of the coliform group: their suitability as markers of microbial water safety. Annu. Rev. Microbiol. 55, 201-234. doi: 10.1146/annurev.micro.55.1.201
35. Ledenbach, L. H., and Marshall, R. T. (2009). "Microbiological spoilage of dairy products, " in Compendium of the Microbiological Spoilage of Foods and Beverages, eds W. H. Sperber and M. P. Doyle (New York, NY: Springer Science+Business Media), 41-67.
36. Lawrence, J. C., and Lilly, H. A. (1972). A quantitative method for investigating the bacteriology of skin: its application to burns. J. Exp. Pathol. 53, 550-555.
37. Macedo, A. C., and Malcata, F. X. (1997). Role of adventitious microflora in proteolysis and lipolysis of serra cheese: preliminary screening. Z. Lebensm. Unters. Forsch. A. 205, 25-30. doi: 10.1007/s002170050118
38. Marchand, S., DeBlock, J., DeJonghe, V., Coorevits, A., Heyndrickx, M., and Herman, L. (2012). Biogilm formation in milk production and processing environments; influence on milk quality and safety. Compreh. Rev. Food Sci. Food Saf. 11, 133-147. doi: 10.1111/j.1541-4337.2011.00183.x
39. Martin, N. H., Carey, N. R., Murphy, S. C., Wiedmann, M., and Boor, K. J. (2012). A decade of improvement: New York State fluid milk quality. J. Dairy Sci. 95, 7384-7390. doi: 10.3168/jds.2012-5767
40. Martin, N. H., Ranieri, M. L., Murphy, S. C., Ralyea, R. D., Wiedmann, M., and Boor, K. J. (2011). Results from raw milk microbiological tests do not predict the shelf-life performance of commercially pasteurized fluid milk. J. Dairy Sci. 94, 1211-1222. doi: 10.3168/jds.2010-3915
41. Masiello, S. N., Martin, N. H., Trmcic, A., Wiedmann, M., and Boor, K. J. (2016). Identification and characterization of psychrotolerant coliform bacteria isolated from pasteurized fluid milk. J. Dairy Sci. 99, 130-140. doi: 10.3168/jds.2015-9728
42. Massa, S., Poda, G., Cesaroni, D., and Trovatelli, L. D. (1989). A bacteriological survey of retail ice cream. Food Microbiol. 6, 129-134. doi: 10.1016/S0740-0020(89)80020-6
43. M-E-Elahi, A. T. M., Habib, S., Rahman, M. M., Rahman, G. I., and Bhulyan, M. J. U. (2002). Sanitary quality of commercially produced ice cream sold in the retail stores. Pakistan J. Nutr. 1, 93-94. doi: 10.3923/pjn.2002.93.94
44. Morales, P., Fernandez-Garcia, E., and Nunez, M. (2003). Caseinolysisin cheese by Enterobacteriaceae strains of dairy origin. Lett. Appl. Microbiol. 37, 410-414. doi: 10.1046/j.1472-765X.2003.01422.x
45. Nornberg, M. F. B. L., Friedrich, R. S. C., Weiss, R. D. N., Tondo, E. C., and Brandelli, A. (2009). Proteolytic activity among psychrotrophic bacteria isolated from refrigerated raw milk. Int. J. Dairy Technol. 63, 41-46. doi: 10.1111/j.1471-0307.2009.00542.x
46. Nunez, M., Gaya, P., and Medina, M. (1985). Influence of manufacturing and ripening conditions on the survival of Enterobacteriaceae in manchego cheese. J. Dairy Sci. 68, 794-800. doi: 10.3168/jds.S0022-0302(85)80894-8
47. Pantoja, J. C. F., Reinemann, D. J., and Ruegg, P. L. (2011). Factors associated with coliform count in unpasteurized bulk milk. J. Dairy Sci. 94, 2680-2691. doi: 10.3168/jds.2010-3721
48. Parr, L. W. (1938). Coliform intermediates in human feces. J. Bacteriol 36, 1-15.
49. Quigley, L., O'Sullivan, O., Beresford, T. P., Ross, R. P., Fitzgerald, B. F., and Cotter, P. D. (2011). Molecular approaches to analysing the microbial composition of raw milk and raw milk cheese. Int. J. Food Microbiol. 150, 81-94. doi: 10.1016/j.ijfoodmicro.2011.08.001
50. Ralyea, R. D., Wiedmann, M., and Boor, K. J. (1998). Bacterial tracking in a dairy production system using phenotypic and ribotyping methods. J. Food Prot. 61, 1336-1340.
51. Ranieri, M. L., and Boor, K. J. (2009). Short communication: bacterial ecology of high-temperature, short-time pasteurized milk processed in the United States. J. Dairy Sci. 92, 4833-4840. doi: 10.3168/jds.2009-2181
52. Ranieri, M. L., Huck, J. R., Sonnen, M., Barbano, D. M., and Boor, K. J. (2009). High temperature, short time pasteurization temperatures inversely affect bacterial numbers during refrigerated storage of pasteurized fluid milk. J. Dairy Sci. 92, 4823-4832. doi: 10.3168/jds.2009-2144
53. Schvartzman, M. S., Gonzalez-Barron, U., Butler, F., and Jordan, K. (2014). Modeling the growth of Listeria monocytogenes on the surface of smear-or mold-ripened cheese. Front. Cell. Infect. Microbiol. 4:90. doi: 10.3389/fcimb.2014.00090
54. Seidler, R. J., Knittel, M. D., and Brown, C. (1975). Potential pathogens in the environment: cultural reactions and nucleic acid studies on Klebsiella pneumoniae from clinical and environmental sources. Appl. Microbiol. 29, 819-825.
55. Tortorello, M. (2003). Indicator organisms for safety and quality-uses and methods for detection: minireview. J. AOAC Int. 86, 1208-1217.
56. Trmcic, A., Chauhan, K., Kent, D. J., Ralyea, R. D., Martin, N. H., Boor, K. J., et al. (2016). Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection. J. Dairy Sci. 99, 1-16. doi: 10.3168/jds.2016-11112
57. Van Kessel, J. S., Karns, J. S., Gorski, L., McCluskey, B. J., and Perdue, M. L. (2004). Prevalence of Salmonellae, Listeria monocytogenes and fecal coliforms in bulk tank milk on US dairy farms. J. Dairy Sci. 87, 2822-2830. doi: 10.3168/jds.S0022-0302(04)73410-4
58. Van Tassell, J. A., Martin, N. H., Murphy, S. C., Wiedmann, M., Boor, K. J., and Ivy, R. A. (2012). Evaluation of various selective media for the detection of Pseudomonas species in pasteurized milk. J. Dairy Sci. 95, 1568-1574. doi: 10.3168/jds.2011-4958
59. Warke, R., Kamat, A., Kamat, M., and Thomas, P. (2000). Incidence of pathogenic psychrotrophs in ice creams sold in some retail outlets in Mumbai, India. Food Control 11, 77-83. doi: 10.1016/S0956-7135(99)00027-4
60. Wessels, D., Jooste, P. J., and Mostert, J. F. (1989). Psychrotrophic, proteolytic and lipolytic properties of Enterobacteriaceae isolated from milk and dairy products. Int. J. Food Microbiol. 9, 79-83. doi: 10.1016/0168-1605(89)90040-8
61. Wolfe, B. E., Button, J. E., Santarelli, M., and Dutton, R. J. (2014). Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158, 422-433. doi: 10.1016/j.cell.2014.05.041