Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection.
Coliform detection in finished products, including cheese, has traditionally been used to indicate whether a given product has been manufactured under unsanitary conditions. As our understanding of the diversity of coliforms has improved, it is necessary to assess whether coliforms are a good indicator organism and whether coliform detection in cheese is associated with the presence of pathogens. The objective of this study was (1) to evaluate cheese available on the market for presence of coliforms and key pathogens, and (2) to characterize the coliforms present to assess their likely sources and public health relevance. A total of 273 cheese samples were tested for presence of coliforms and for Salmonella, Staphylococcus aureus, Shiga toxin-producing Escherichia coli, Listeria monocytogenes, and other Listeria species. Among all tested cheese samples, 27% (75/273) tested positive for coliforms in concentrations >10cfu/g. Pasteurization, pH, water activity, milk type, and rind type were factors significantly associated with detection of coliforms in cheese; for example, a higher coliform prevalence was detected in raw milk cheeses (42% with >10cfu/g) compared with pasteurized milk cheese (21%). For cheese samples contaminated with coliforms, only water activity was significantly associated with coliform concentration. Coliforms isolated from cheese samples were classified into 13 different genera, including the environmental coliform genera Hafnia, Raoultella, and Serratia, which represent the 3 genera most frequently isolated across all cheeses. Escherichia, Hafnia, and Enterobacter were significantly more common among raw milk cheeses. Based on sequencing of the housekeeping gene clpX, most Escherichia isolates were confirmed as members of fecal commensal clades of E. coli. All cheese samples tested negative for Salmonella, Staph. aureus, and Shiga toxin-producing E. coli. Listeria spp. were found in 12 cheese samples, including 5 samples positive for L. monocytogenes. Although no association was found between coliform and Listeria spp. detection, Listeria spp. were significantly more likely to be detected in cheese with the washed type of rind. Our data provide information on specific risk factors for pathogen detection in cheese, which will facilitate development of risk-based strategies to control microbial food safety hazards in cheese, and suggest that generic coliform testing cannot be used to assess the safety of natural cheese.
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
A
A
Trmčić
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
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K
Chauhan
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
D J
DJ
Kent
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
R D
RD
Ralyea
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
N H
NH
Martin
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850.
K J
KJ
Boor
Milk Quality Improvement Program, Department of Food Science, Cornell University, Ithaca, NY 14850. Electronic address: mw16@cornell.edu.
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M
Wiedmann
D000818:Animals; D002611:Cheese / Q000032:analysis* / Q000382:microbiology*; D004755:Enterobacteriaceae / Q000302:isolation & purification*; D005243:Feces / Q000382:microbiology; D005511:Food Handling / Q000379:methods; D005513:Food Inspection / Q000379:methods; D005516:Food Microbiology; D006863:Hydrogen-Ion Concentration; D008089:Listeria monocytogenes / Q000302:isolation & purification; D008892:Milk / Q000382:microbiology; D061352:Pasteurization; D012475:Salmonella / Q000302:isolation & purification; D054323:Shiga-Toxigenic Escherichia coli / Q000302:isolation & purification; D013211:Staphylococcus aureus / Q000302:isolation & purification; D014867:Water / Q000032:analysis
D014867:Water
cheese; coliform; fecal contamination; pasteurization; pathogen