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Cheese Safety 101

Part 2: I have seen the enemy and he speaks Latin

Art Hill and Keith Warriner
Department of Food Science
University of Guelph,
Guelph, ON, N1G 2W1
arhill@uoguelph.ca

Molly Sandvick of Seattle, will not soon forget a Latin name she learned in Victoria, BC. That's where Sandvick, who was pregnant at the time, contracted listeriosis from cheese contaminated with Listeria monocytogenes, an illness that caused her to lose the baby (Vancouver Sun, March 21, 2023). This article describes Listeria monocytogenes and other enemies of cheese, all with Latin names. Let's start with a little review.

Part 1 of Cheese Safety 101 described risk as the product of the severity of the consequences and the probability of a negative event, such as falling off a ladder or consuming food contaminated with pathogenic (illness causing) microorganisms.

Risk = (severity of the event) x (probability of the event)

We explained that effective product tracking and recall protocols are important to reduce the severity (the extent) of a food borne illness out break if it should occur. However, this series of articles on cheese safety is concerned mainly with technological principles of particular relevance to cheese making that can be applied to reduce the probability of food borne illness events to near zero. In other words, we're going to work mainly on the second part of the equation.

Specifically, the purpose of this article, Part 2 in the series, is to characterize the microbial pathogens that occur in raw milk and may persist during cheese making and ripening. Plant and personnel hygiene is important to prevent cheese contamination with other pathogenic microbial agents such as cryptosporidium and viruses such as Hepatitis A, but these will not be discussed here.

Table 1 lists some properties of the pathogenic microorganisms of most concern to cheese makers. Please interpret the data 'with a grain of cheese salt'. All the parameters described depend on many factors, so, the literature values cited must be interpreted as very approximate. For those who want to investigate further, the list of literature references is available here. Useful web links are the Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration and the U.S. Center for Disease Control. The importance of acid tolerance (pH), growth temperature and other parameters in Table 1 will become more clear with subsequent articles, so please keep it handy for future reference.

The bacteria in Table 1 are listed in order of decreasing concern for cheese safety, where risk is estimated by the authors. Some food safety experts may order them differently, but there is little doubt that the first three in the list, Listeria monocytogenes, Salmonella species and enteropathogenic Escherichia coli represent the greatest concern for cheese makers1.

In our estimate, Listeria monocytogenes represents the highest risk because both the severity and probability of listeriosis are high relative to other food borne diseases associated with cheese. On the severity side of the equation, death rate associated with listeriosis is about 30%, and for those who survive, there may be serious complications such as spontaneous abortion. On the probability side of the equation, the rate of incidence of Listeria monocytogenes in raw milk is relatively high, its thermal tolerance is close to pasteurization (72°C, 16 s), it survives if not thrives under the conditions of cheese making, and it is able to grow at refrigeration temperatures (i.e., cheese ripening and storage temperatures).

Similarly, Salmonella species and Eshericia coli O157 H7 are listed as high risk because they are frequently present in raw milk, they grow at or at least tolerate cold temperatures and acidity in the range of cheese and other fermented milk products, and they may persist for several months during ripening.

Staphylococcus aureus is a frequent contaminant in cheese, from raw milk or from personnel, but was listed as low risk because growth and toxin production are readily suppressed by lactic cultures and acidity (reduced pH) in cheese 1.

Campylobacter jejuni is wide spread in the environment and occurs in raw milk, but does not normally survive cheese making conditions. So, it's considered low risk for cheese making provided that one of heat treatment or fermentation (reduced pH) are included in the cheese process.

Yersinia enterocolitica apparently tolerates cheese making conditions and according to many studies occurs frequently in milk. However, recent studies suggest that virulent strains, especially in North America occur less frequently 3,4. Also U.S. Centre for Disease Control statistics confirm that Yersinia outbreaks are rare in the U.S. 2.

Bacillus cereus is a nuisance because it forms difficult to remove bacterial films on milk processing equipment, survives pasteurization and grows well at refrigeration temperatures. However, it is considered low risk because production of diarrheal toxin in milk is associated with obvious spoilage and cell counts greater than 10 million 5,6. It's interesting to note that pasteurization of milk encourages germination of Bacillus cereus spores so its numbers may be higher in pasteurized milk than in raw milk 7,8.

OK, so, with that brief introduction to the 'enemy', what are the take-home points?

The good news is the incidence of food poisoning associated with cheese is, apparently, according to the outbreaks listed by the U.S. Centre for Disease Control 2 low relative to other food products.

The bad news is that a substantial portion of raw milk is contaminated with one or more pathogenic microorganisms. Using the rules of probability and the average incidence rates reported in column three of Table 1, we estimate (crudely) that about 12% of cow milk is contaminated with one or more of Listeria monocytogenes, Salmonella species and Esherichia coli O157 H7 before it leaves the farm. A South Dakota study that found 26% of bulk tank samples were contaminated with one or more of Eshericia coli O157 H7, Listeria monoctyogenes, Salmonella spp. and Campylobacter jejuni9. In Tennessee, 25% of bulk tanks were contaminated with one or more of Listeria monocytogenes, Campylobacter jejuni, Yersinia enterocolitica and Salmonella species 38. The pooling process during milk transport and storage ensures that the proportion of contaminated milk reaching the cheese vat is usually much higher.

In conclusion, the cheese maker must assume that the raw milk destined for cheese making is contaminated with one or more pathogenic bacteria. That's true even if the milk is from your own farm. It is critical to approach cheese making with assumption that pathogen bacteria are present in the milk and must be eliminated during the cheese making process. One ally of the cheese maker in the war on cheese pathogens is acidity. That's the topic of Part 3 in this series. Stay tuned!

Table 1. Some properties of pathogenic bacteria occurring in milk and dairy products. Numbers in brackets refer to a reference list available here. Unreferenced data are 'educated' estimates based on experience and unpublished information.

Organism Properties Incidence in raw milk
Listeria monocytogenes
  • Infectious dose typically over 10 M but may be as few as 1000 cells2
  • Onset time: 12 h to several weeks2
  • Temperature range: 1-3C10,11
  • Minimum pH: 4.412
  • Heat resistance:1 67-72°C, 15- 16 s13,14
  • Survives up to 27 d in yoghurt15
  • Survives mesophilic cheese making and slowly declines during ripening15
  • May accumulate in surface ripened cheese environments during ripening16
  • Symptoms more severe than other pathogens likely to occur in cheese; 30% mortality, spontaneous abortion2.
  • 1.5% Germany17
  • Ontario 1.3%18, 8.2%19, 2.7%20
  • Alberta 9-11%21
  • Unknown 3.9%22
  • Tennessee 4.1%38
  • Spain 3.62%23
  • Ireland 53%24, 4.9%25
  • England and Wales 5%26
  • US 6.5%27
  • Sweden 1.0%28
  • Incidence in goat milk: US 3.8%29Spain 2.56%23
  • Incidence in sheep milk: 2.2%30
Salmonella, many species.
S. enteritidis, is most common in cheese31.
  • Infectious dose typically over 100 10,000 cells, may be as few as 15 -20 cells 2,32
  • Onset time: 6 to 48 hours2
  • Growth range : 5 - 47C33
  • Minimum pH: 3.9 4.034,35
  • Heat resistance: 62- 68C, 16 s36
  • Survives mesophilic cheese making and slowly declines during ripening37
  • Germany 0%17
  • England and Wales 0.36%26
  • Tennessee 8.9%38
  • Ontario 0.17%20
  • US 2.6%27
Esherichia Coli O157 H7. Other illness causing E. coli rarely occur in dairy products and are less virulent than O157 H7.
  • Infective dose may be as low as 10 cells; illness due to Enterotoxins2
  • Onset time: Two to four days
  • Minimum growth temperature: 4C39
  • Minimum growth pH: 3.840
  • Heat resistance:1 65C, 16 s36
  • Germany 1.5%17, 15.1%38
  • Ontario 0.87%20
Enterotoxigenic Staphylococcus aureus
  • Illness due to heat stable toxic protein. About 100,000 bacteria/g produce sufficient toxin to cause illness2
  • Onset time: 1-6 h
  • Temperature range for growth: 6-45C; toxin production 30-37C.
  • Minimum pH: 5.0
  • Rapidly declines during cheese making and ripening.
  • Incidence: goat milk: 10% Italy41
  • Cheese contamination also commonly occurs due to poor personnel hygiene.
Campylobacter jejuni
  • Infectious dose: 400 bacteria2
  • Onset time 2 - 5 d2
  • Growth temperature range: 30 45C42
  • Minimum pH: 5.542
  • Heat resistance:63C, 16 s36
  • Germany 2.3%17
  • Egypt 7%43
  • Tennessee 12.3%38
  • Ontario 0.47%20
  • Difficult to isolate and enumerate, so reported incidence may be under estimated.
Yersina enterocolitica
  • Infectious dose, unknown but probably low.
  • Onset time 24-48 h2
  • Temperature growth range is not known, but survives for substantial periods in chilled foods.
  • Acid tolerance is not known but it does survive in fermented milk products: survived in kefir for 14 days versus 21 days for Listeria monocytogenes44,45
  • Heat resistance:1 63C, 16 s36
  • Several studies show high incidence, 5-23% in milk 9,25,38,46-49 and goat milk50
  • Recent studies highlight difficulties of identifying virulent strains and suggest incidence of virulent strains is low: 0.9% 3,4
Bacillus cereus
  • Toxicity due to protein causing diarrhea OR heat stable emetic (vomiting) toxin. The emetic type is rare in milk51. About 10 M cells/g required to cause illness2.
  • Incubation period: 6 to 15 h2.
  • Diarrheal strains grow and produce toxin at 4-7C5,52,53
  • Minimum pH: 5.5
  • Heat resistance: Forms spores that survive pasteurization; diarrheal toxin also survives pasteurization; (72C, 16 s)54
  • Forms difficult to clean microscopic films on processing surfaces
  • Unknown 3.8%55
  • Scotland 18%56