On September 25, 2009, I posted Part 1 of a 4-part series that examines the food safety record of both pasteurized and raw dairy products. Below is Part 2, which provides background on the occurrence of foodborne pathogens in milk products, and mechanisms of contamination.
Occurrence of Foodborne Pathogens in Milk and the Dairy Environment
Dairy animals such as cattle and goats may carry foodborne pathogens (e.g., Campylobacter, E. coli O157:H7, Listeria monocytogenes, Salmonella; see “cons” for a more extensive list). Often cows and goats that harbor foodborne pathogens in their gastrointestinal tracts do not appear to be ill. Occasionally, some of these bacteria cause mastitis (infection and inflammation of the udder), and may be shed directly into the milk. Certain strains of Salmonella and Listeria monocytogenes can cause serious systemic illness in ruminants. For example, Salmonella Dublin is a strain that is host adapted to cattle, and can lead to severe diarrhea and death in both cattle (especially calves) and humans.
Several authors have conducted extensive surveys of foodborne pathogens in bulk tank raw milk (BTM) and the dairy environment (Hancock et al 1998; Jayarao et al, 2006; LeJeune et al, 2009; Oliver et al, 2005; Oliver et al, 2005; Shere et al, 1998). BTM is milk from multiple cows mixed and stored in a container. Modern conventional dairies usually ship their milk in tanker trucks off-site for pasteurization. Milk from multiple farms may be mixed together. The majority of milk produced for pasteurization comes from confined animal feeding operations (CAFOs). In contrast, most commercial raw milk produced for human consumption in the US comes from pasture-based management systems as promoted by the Weston A. Price Foundation (WAPF). Milk from multiple cows may be mixed together and stored in a container, but raw milk from multiple farms is not usually combined. An exception would be “outsourcing” where the dairyman purchases additional milk from surrounding dairies to meet supply needs. This practice is probably uncommon, but considered dangerous because outsourced milk is not produced as required for the Grade A raw milk designation.
The most recent review of the literature on foodborne pathogens in BTM was published by Oliver et al (2009). The range in prevalence for BTM was summarized as follows:
Campylobacter: 2 – 9.2%
E. coli O157:H7: 0 – 0.75%
Listeria monocytogenes: 2.8 – 7.0%
Salmonella spp: 0 – 11%
Shiga-toxin E. coli: 2.4 – 3.96%
Yersinia enterocolitica: 1.2 – 6.1%
WAPF has raised a valid concern about using these surveys when assessing the occurrence of foodborne pathogens in commercial raw milk (e.g., raw milk sold legally on- or off-farm in the US). Because the BTM tested in these surveys was likely destined for pasteurization, the data does not specifically address the microbial quality or pathogen prevalence in Grade A raw milk sold for human consumption. Additional research is needed that compares BTM samples from licensed raw milk dairies to BTM intended for pasteurization. Furthermore, to fully understand the risk of pathogen contamination in raw milk being purchased and consumed in the US, surveys are needed that examine the prevalence of foodborne pathogens in raw milk produced by licensed, inspected raw dairies; unlicensed, “black market” raw dairies; and raw dairies selling their products as “pet food.”
Raw Bovine Colostrum
Colostrum is the “first milk” produced by the mammary gland of an animal after giving birth. Consumption of raw bovine colostrum appears to be increasing in popularity among raw milk drinkers, and has been associated with two recent foodborne disease outbreaks in California (CDC 2008; CDPH 2008). Unlike raw milk, raw bovine colostrum is regulated as a nutritional supplement. A recent survey of dairies in Pennsylvania by Houser et al (2008) found Salmonella in 15% of the colostrum samples; the mean standard plate counts (SPC) and coliforms were very high: 977,539 CFU/ml and 323,372 CFU/ml, respectively (see Oliver et al, 2009, for a broader discussion of sanitation standards). It was not specified in the paper if these dairies surveyed in Pennsylvania sold raw bovine colostrum for human consumption. Additional surveys are needed to study foodborne pathogens and sanitary standards in raw bovine colostrum from dairies that market the product as a nutritional supplement for humans.
Addressing the WAPF Claim: “Clean Grass Fed Cows” are Safe
WAPF and their Chapter members strongly promote the idea to their customers that raw milk is safe if produced by “clean grass fed cows.” Yet, the organization does not provide any survey data to support these claims. The only studies that potentially relate are found in the literature on grass vs. grain feeding and prevalence of E. coli O157:H7. This topic was reviewed previously. Briefly, the scientific evidence at this time does not support a broad conclusion that grass feeding significantly and consistently reduces the risk of E. coli O157:H7 or other dangerous foodborne pathogens from entering the food chain. More importantly, none of the surveys or experiments that WAPF cites examined raw milk operations, and instead focused primarily on dietary effects for cattle in feedlot conditions.
Most of the data on foodborne pathogen occurrence in the raw milk dairy environment comes from outbreak investigation reports. There are several examples where foodborne pathogens were found in the milk, cattle feces, and/or milking barn at dairies that follow WAPF principles including pasture-based, grass only feeding. In 2005, Washington state investigated an outbreak of E. coli O157:H7 linked to a cow-share, and found the outbreak strain in raw milk and environmental samples at the dairy (CDC 2007). In 2006, retail raw milk and colostrum were implicated in an outbreak of E. coli O157:H7 among children in California (CDC 2008). The outbreak strain was not found on the farm, but E. coli O157:H7 was present in the herd. In 2007, Campylobacter jejuni was isolated from 35% of fecal samples from cows at that same dairy in California; the outbreak strain was found in 4 fecal samples from those cows (CDPH 2008).
Addressing the WAPF Claim: Raw Milk Kills Pathogens
Another unsubstantiated claim by WAPF relates to the idea that raw milk is safe because the “good” bacteria and specific components in the unheated milk will destroy pathogens. A comprehensive review of this topic is beyond the scope of this paper. Briefly, the evidence that WAPF uses to promote this claim comes primarily from a paper by Doyle and Roman (1982) where Campylobacter jejuni was found to die-off at a more rapid rate in raw milk compared with sterile milk. However, the number of C. jejuni organisms in raw milk did not drop to a level below the infectious dose until about 7 days after inoculation. Furthermore, most C. jejuni stains also died-off in sterile milk, but not until a couple days later. WAPF does not make this distinction when promoting the safety of raw milk. Another consideration not addressed adequately by WAPF in their claims about raw milk safety is the importance of temperature abuse. Both raw and pasteurized milk are rich in nutrients, and if stored above refrigeration temperatures, can serve as an excellent medium for growth of pathogens (Wang et al, 1997).
A more extensive discussion on competitive exclusion and consumer perceptions was recently published by Rose (2009) as a White Paper.
How is Milk Contaminated with Pathogens?
There are 3 important points to consider about how milk becomes contaminated:
1. The initial mechanisms for raw milk contamination with pathogens are the same whether the milk is destined to be consumed raw, or pasteurized:
• Mastitis and shedding of the pathogen directly from the cow’s udder into the milk
• Entry of manure or dirt into the milk during the milking process
• Transfer of pathogens by vectors if they come in contact with the raw milk (for example, flies may carry pathogens on their legs and mouthparts)
• Human carriers transferring pathogens from their hands to the milk
2. The major difference between raw and pasteurized milk is the fact that the heat treatment during pasteurization destroys pathogens that may have entered the raw milk as described above.
3. Both raw and pasteurized milk can be contaminated during bottling, shipment, and storage. Pasteurization only destroys the pathogens in the milk at the time of processing; if unsanitary conditions allow pathogens to re-enter the milk later, it will be contaminated again.
There are two general causes of contamination of pasteurized milk:
1. Equipment failure: The pasteurization equipment fails and there is raw milk in the product sold as pasteurized. This can happen if the temperature is not high enough, or if the milk is not heated long enough. For example, in 1984, an outbreak of Salmonella Typhimurium occurred in a convent in western Kentucky (CDC, 1984). There were 16 illnesses and one patient developed a Guillain-Barre-type illness. The convent had a steam pasteurizer and investigators believe that the temperature may not have been high enough and/or the holding time was too short. The convent had no time-temperature gauge to record and monitor the process.
2. Post-pasteurization contamination: the milk is contaminated after pasteurization, usually through unsanitary handling of the milk. An example of post-pasteurization contamination involving a multi-drug resistant strain of Salmonella Typhimurium occurred in Pennsylvania and New Jersey in 2000 (Olsen et al, 2004). There were 93 illnesses and at least 6 hospitalizations. No Salmonella was isolated from the milk, but investigators concluded that the milk was most likely contaminated after pasteurization due to unsanitary conditions at the processing plant. For example, high humidity and excessive condensation in the plant could have produced droplets carrying Salmonella that fell into open containers of the pasteurized milk.
In the Age of Bioterrorism
Intentional contamination of the food supply through a bioterror attack has become an increasing concern. Wein and Liu published a provocative paper in 2005, where they modeled the vulnerability of pasteurized milk though the farm-to-consumer supply chain using botulinum toxin. They considered milk a possible target because of its symbolic value in society. The authors concluded that due to the rapid distribution and consumption of milk, an attack could result in several hundred thousand individuals poisoned with botulinum toxin.
It is worth noting that the conventional pasteurized milk supply is far more vulnerable to a massive poisoning compared with today’s raw milk supply. Several enormous, natural foodborne disease outbreaks involving pasteurized dairy products illustrate this point (Ryan et al, 1987; Hennessy et al, 1996). However, recent petitions to FDA to expand the raw milk supply chain by lifting the interstate ban on shipment could potentially increase the vulnerability of raw milk to larger outbreaks because a single contaminated lot would be consumed by many more individuals across a wider geographic area.
“Good” vs. “Bad” Bacteria: Probiotics and Dairy Products
One of the major concerns expressed by WAPF and other raw milk advocacy groups is that heat treatment by pasteurization destroys “good bacteria,” as well as pathogens. An example of “good” bacteria would be probiotics. A simple definition of a probiotic is a live microorganism (such as Bifidobacteria and Lactobacilli) that is beneficial to health when consumed. An example of a benefit from probiotics would be improved digestion.
Although raw milk may contain “good bacteria,” it is debatable whether raw dairy products fit the scientific definition of a probiotic food (see my previous review on Raw Milk Pros). Animals do not excrete “good bacteria” in their milk (usually milk is sterile when it exits the mammary gland). Both “good” and “bad” bacteria enter milk by the same mechanisms as described above. Sanitation during milking and processing at a raw milk dairy to prevent pathogens from entering the milk will very likely also lower the levels of probiotic bacteria. The ultimate question for the consumer is whether the trade off is worth the risk. It is worth noting that there is very little research on this topic. For example, studies are needed to measure the species and concentration of “good” bacteria in commercial raw dairy products to determine if they are sufficient to confer a probiotic effect.
In recent years, pasteurized dairy products containing probiotic bacteria have become increasingly popular. Products such as Activia® and DanActive® contain specific species and numbers of live probiotic microorganisms that are added to the dairy product after pasteurization to kill harmful bacteria.
The next segment of this review will compare foodborne illnesses and disease outbreaks linked to raw and pasteurized dairy products.
1. CDC. 2007. Escherichia coli O157:H7 infection associated with drinking raw milk—Washington and Oregon, November – December 2005. MMWR Morb Mortal Wkly Rep 56:165-7.
2. CDC. 2008. Escherichia coli 0157:H7 Infections in Children Associated with Raw Milk and Raw Colostrum From Cows — California, 2006. MMWR Morb Mortal Wkly Rep 57:625-8.
3. CDC. 1984. Salmonellosis from inadequately pasteurized milk–Kentucky. MMWR Morb Mortal Wkly Rep 33:505-6.
4. CDPH. 2008. Cluster of Campylobacter infections possibly associated with raw dairy products. Available at: https://www.marlerblog.com/Cluster%20of%20Campylobacter%20infections.pdf
5. Doyle, M. P. and D. J. Roman. 1982. Prevalence and survival of Campylobacter jejuni in unpasteurized milk. Appl Environ Microbiol 44:1154-8.
6. Hancock D. D., T. E. Besser, D. H. Rice, E. D. Ebel, D. E. Herriott, and L. V. Carpenter. 1998. Multiple sources of Escherichia coli O157 in feedlots and dairy farms in the northwestern USA. Prev Vet Med 35:11-9.
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14. Rose, A. 2009. Does raw milk kill pathogens? A visual summary of the research on competitive exclusion. Available at: http://rawmilkwhitepapers.com/
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16. Shere, J. A., K. J. Bartlett, and C. W. Kasper. 1998. Longitudinal study of Escherichia coli O157:H7 dissemination on four dairy farms in Wisconsin. Appl Environ Microbiol 64:1390-9.
17. Wang, G. T. Zhao, and M. P. Doyle. 1997. Survival and growth of Escherichia coli O157:H7 in unpasteurized and pasteurized milk. J Food Protect 60:610-3.
18. Wein, L. M., and Y. Liu. 2005. Analyzing a bioterror attack on the food supply: the case of botulinum toxin in milk. Proc Natl Acad Sci U S A 102:9984-9.