Part 1 and part 2 of this series examined the historical context of the debate surrounding dairy product food safety, and the mechanisms by which pasteurized or raw dairy products may become contaminated with foodborne pathogens. This section compares foodborne illnesses and disease outbreaks linked to raw and pasteurized dairy products.
Several sources were used to analyze the available data including Centers for Disease Control and Prevention (CDC) foodborne disease outbreak surveillance tables, an online outbreak database published by the Center for Science in the Public Interest (CSPI), public health reports such as the Morbidity and Mortality Weekly (MMWR), peer-reviewed manuscripts, and CDC Line List of dairy outbreaks from 1973-2005 produced in response to a Freedom of Information Act (FOIA) request to CDC by the Farm to Consumer Legal Defense Fund (FTCLDF).
These data sources are useful in comparing trends and potential risk factors, but several limitations must be noted. First, not all foodborne illnesses are reported to CDC as described by Mead et al (1999). For example, two notable outbreaks in California are missing from both the CDC and CSPI databases: a large outbreak of campylobacteriosis in 2006, involving over 1,644 illnesses among inmates that was linked to pasteurized milk produced by an on-site prison dairy (Jay et al, 2007) and another campylobacteriosis outbreak in 2007, that caused 8 illnesses following consumption of commercial raw milk and/or raw colostrum (CDPH 2008). There are additional examples of discrepancies between the CDC surveillance line listings, public health reports, and the peer-reviewed literature; however, these differences exist for both raw and pasteurized milk, as well as other food products. Second, state and local health departments vary in the level of resources available for foodborne disease outbreak investigations; therefore, some outbreaks are investigated more intensively than others. Given all of these considerations, there is no indication of a “systematic bias” against raw milk, as suggested by the Weston A. Price Foundation (WAPF).
Foodborne Disease Surveillance and Outbreak Investigation: The Smoking Gun
A major misconception by WAPF is that outbreak investigations involving raw milk are conducted in a substantially different (and biased) way compared with the techniques used for pasteurized milk, or other foods (e.g., spinach, deli meats, ground beef, etc.). In reality, outbreaks from raw and pasteurized milk are investigated using the same approaches, and both are subject to the same limitations as described above.
Below are some examples of misleading statements from WAPF in their response to outbreak papers cited in the Raw Milk Cons review:
“When they tested the milk for C. jejuni, however, none could be found…Over and over again, investigators blame C. jejuni outbreaks on raw milk despite negative milk samples.”
Isolation of the “outbreak strain” from a food product provides strong support (“The Smoking Gun”) for epidemiological studies implicating the same food; however, a positive food sample is not a requirement to take action to prevent new illnesses (e.g., recall and/or stopping distribution of an epidemiologically implicated food). Often, there is no leftover food product to test, especially if it is perishable such as milk or produce. Or, the test may be negative because the pathogen already died-off in the leftover milk due to the lag between the time the patient drank the milk and the time the outbreak investigation started.
Despite these limitations, the “outbreak strain” has been isolated from raw milk during investigations (Table 1, Figure 1a). Likewise, many examples of pasteurized milk-related outbreaks exist where milk samples tested negative (Table 2, Figure 1b), but investigators still concluded that the pasteurized milk was the most likely source. Note that when resources permit, DNA fingerprinting is used during both pasteurized and raw milk outbreak investigations to compare isolates from patients, milk products, and the farm environment.
“VERDICT: no evidence of illness”
WAPF repeatedly uses this phrase when dismissing a raw milk-related outbreak, usually citing negative milk sample tests. Yet, they do not provide any caveats or dismissals of pasteurized milk–related outbreak investigations where milk testing results were negative. This double standard used by WAPF is inherently biased, and could mislead consumers. Their press release concerning a recent campylobacteriosis outbreak in Wisconsin illustrates this point.
“Finally, most studies associating raw milk with illness never pinpoint where along the line of production the contamination occurred.”
In most dairy outbreaks, regardless of pasteurization status, the exact mechanism of contamination is never found. However, a commonality in virtually all milkborne outbreaks is sanitation. Dairies are not clean environments, regardless of whether it is a small “grass fed” farm, or a large CAFO. Cows produce copious amounts of manure, and can readily contaminate the milking parlor and equipment (Figures 1a and 1b). Sanitation can also be a major problem during the production of Mexican-style soft cheeses such as queso fresco (Figure 1c).
Figure 1a. Photo taken during the investigation of a raw milk-associated E. coli O157:H7 outbreak in Washington State, 2005. Eighteen illnesses including 4 cases of HUS were linked to “grass fed” raw milk from an unlicensed cow-share program. The farm milked 5 cows in a parlor with a dirt floor and mats shown in the photo. The outbreak strain was isolated from raw milk and floor samples. Investigators concluded that unsanitary conditions contributed to the outbreak (CDC 2007).
Figure 1b. Photo taken during the investigation of a pasteurized milk-associated Campylobacter jejuni outbreak in California, 2006. Over 1,600 illnesses at 11 state correctional facilities were linked to drinking pasteurized milk supplied by an on-site dairy at one of the prisons. The inmates milked ~500 cows in a parlor adjacent to the pasteurization building. The outbreak strain was isolated from recycled wastewater shown in the photo (lagoon water is being “flushed” through the cow stall barn). Investigators did not determine how the milk was contaminated after pasteurization, but suggested the need for further evaluation of manure management practices on the dairy (Jay et al, 2007).
Figure 1c. Photo of queso fresco, a Mexican-style soft cheese sometimes produced illegally under unsanitary conditions (“bathtub cheese”). In 2000-2001, an outbreak caused by Listeria monocytogenes involving 12 illnesses, 5 still births, 3 premature deliveries, and 2 infected newborns was associated with consumption of Mexican-style cheese made from raw milk in North Carolina. The cheese was manufactured illegally, and the “outbreak strain” was found in 4 cheese samples and raw milk taken from the farm that supplied the milk (CDC 2001).
A combination of data sources were used to create Table 1 (raw milk outbreaks) and Table 2 (pasteurized milk outbreaks). Oliver et al (2009) also recently published tables showing reports of raw and pasteurized milk outbreaks from 2000-2007. Additional references on raw milk-related illnesses and outbreaks were documented last year in the raw milk cons paper, and Kansas State University and Cornell University have compiled online listings of raw milk-related outbreaks.
Taken together, the data shows that both pasteurized and raw milk products can be important sources of foodborne illness. However, as discussed in Part 1 of this series, dairy products as a whole currently cause the fewest outbreaks of all the major food categories (e.g, beef, eggs, poultry, produce, seafood) (CSPI 2008).
Results from FTCLDF FOIA Request Analysis
A more in-depth analysis of the outbreaks was conducted using the Line List from CDC obtained through a FTCLDF FOIA request. This dataset was chosen because WAPF and other raw milk advocacy groups often refer to it. The data sent by CDC included “Year,” “Estimated Total (illnesses),” “Food,” and “Pathogen.” This information was entered into an Excel file, and a new variable was added called “Category.”
For several outbreaks, the line listing did not specify if the “Food” was “raw/unpasteurized” or “pasteurized.” For example, the food is listed as just “milk” or “chocolate milk.” For the purpose of this analysis, an assumption was made that the unspecified foods were most likely pasteurized products.
A total of 134 outbreaks were listed from 1973-2005, mostly from bacterial causes. Figure 2 shows the number of outbreaks and percentages by “Food” type as originally described in the line listing. Figure 3 shows the number of outbreaks and percentages using the food assigned to three general “Categories:” pasteurized, raw, or queso fresco Mexican-style cheese. Queso fresco was described as a separate category because it is often not known how the product was produced (outbreaks are commonly linked to illegal “bathtub cheese” operations, or illegal imported cheeses from Mexico).
Figure 2. Milkborne disease outbreaks by Food category, United States, 1973-2005 (source: FTCLDF via CDC).
Disproportionate Number of Outbreaks due to Raw Milk Consumption: Only ~1% of people drink raw milk in the United States, yet raw dairy products cause over 50% of the milkborne outbreaks
WAPF and public health officials generally estimate that only 1% of the population drinks raw milk (Headrick et al, 1997). If the risk from raw and pasteurized dairy products was equal, or if raw dairy products were actually safer as WAPF states in their documents, we would expect that raw dairy-related outbreaks would be 1% or less of the total number of outbreaks. Instead, raw dairy products (excluding queso fresco) caused 75 (56%) outbreaks compared with 47 (35%) outbreaks associated with pasteurized milk products (Figure 4). In other words, there should have been only 1-2 raw dairy-related outbreaks among the 134 reported during that time period given the small estimated number of raw milk drinkers.
Figure 3. Milkborne disease outbreaks by food category, United States, 1973-2005 (source: FTCLDF via CDC).
Figure 4. Estimated percentage of people who drink pasteurized and raw milk, United States (Headrick et al, 1997).
Most Pasteurized and Raw Dairy Outbreaks involve less than 50 illnesses
As discussed previously in Part 2, pasteurized milk can be more susceptible to massive outbreaks involving large numbers of illnesses because more consumers drink pasteurized milk, and there is wider distribution of the product. However, outbreaks with more than 1,000 illnesses are relatively rare, and appear to occur about once per decade (Table 2).
An analysis of the illnesses from dairy products using the CDC line listing from FTCLDF is shown in Table 3. The majority of outbreaks for both pasteurized and raw dairy products, as well as queso fresco Mexcian style cheese, usually involved fewer than 50 illnesses. In this database, 4 raw milk outbreaks were associated with over 100 illnesses. Notably, a multi-state outbreak of Salmonella Enteritidis involving over 200,000 illnesses from ice cream (Hennessy et al, 1996) was not listed in this database, possibly due to the fact that cross-contamination of the ice cream by raw eggs during transportation most likely caused the outbreak (thus the outbreak may have been classified as “egg” rather than “dairy” related).
Table 3. Number of illnesses associated with outbreaks due to milk products, 1973-2005 (source: FTCLDF via CDC).
Campylobacter and Salmonella cause the largest number of dairy-related outbreaks
Table 4 shows a breakdown of the reported outbreaks in the FTCLDF CDC line listing by agent (bacterial, viral, or chemical). The majority of outbreaks were due to bacterial pathogens. Notably, Campylobacter was the most common cause of raw milk-related outbreaks with almost 80% attributed to raw milk/cheeses despite claims by WAPF that raw milk “kills” pathogens, especially Campylobacter. Salmonella was the second most commonly reported pathogen overall, and the most frequent agent linked to pasteurized milk outbreaks.
Table 4. Agents causing foodborne outbreaks associated with milk products, 1973-2005 (source: FTCLD via CDC)
The final part of this series will examine more broadly the risks from specific pathogens associated with pasteurized and raw dairy products, and provide consumers information to help them assess these risks when making a decision between consumption of pasteurized and raw dairy products.
1. Ackers, M. L., S. Schoenfeld, J. Markman, M. G. Smith, M. A. Nicholson, W. DeWitt, D. N. Cameron, P. M. Griffin, and L. Slutsker. 2000. An outbreak of Yersinia enterocolitica O:8 infections associated with pasteurized milk. J Infect Dis 181:1834-7.
2. Birkhead, G., R. L. Vogt, E. Heun, C. M. Evelti, and C. M. Patton. 1988. A multiple-strain outbreak of Campylobacter enteritis due to consumption of inadequately pasteurized milk. J Infect Dis 157:1095-7.
3. Black, R. E., R. J. Jackson, T. Tsai, M. Medvesky, M. Shayegani, J. C. Feeley, K. I. MacLeod, and A. M. Wakelee. 1978. Epidemic Yersinia enterocolitica infection due to contaminated chocolate milk. N Engl J Med 298:76-9.
4. CDC. 1966. Shigellosis outbreak – Florida. MMWR Morb Mortal Wkly Rep 15:442.
5. CDC. 1975. A common-source outbreak of Salmonella Newport – Louisiana. MMWR Morb Mortal Wkly Rep 24:413-4.
6. CDC. 1979. Salmonella gastroenteritis associated with milk – Arizona. MMWR Morb Mortal Wkly Rep 28:117-20.
7. CDC. 1984. Salmonellosis from inadequately pasteurized milk–Kentucky. MMWR Morb Mortal Wkly Rep 33:505-6.
8. CDC. 2001. NC2001. From the Centers for Disease Control and Prevention. Outbreak of Listeriosis associated with homemade Mexican-style cheese–North Carolina, October 2000-January 2001. Jama 286:664-5.
9. CDC. 2002. Outbreak of Campylobacter jejuni infections associated with drinking unpasteurized milk procured through a cow-leasing program–Wisconsin, 2001. MMWR Morb Mortal Wkly Rep 51:548-9.
10. CDC. 2003. Multi-state outbreak of Salmonella Serotype Typhimurium infections associated with drinking unpasteruized milk – Illinois, Indiana, Ohio, and Tennessee. 2002-2003. MMWR Morb Mortal Wkly Rep 52:613-5.
11. CDC. 2007a. Escherichia coli O157:H7 infection associated with drinking raw milk – Washington and Oregon. November – December 2005. MMWR Morb Mortal Wkly Rep 56:165-7.
12. CDC. 2007b. Salmonella Typhimurium infection associated with raw milk and cheese consumption – Pennsylvania, 2007. MMWR Morb Mortal Wkly Rep 56:1161-4.
13. CDC. 2008a. 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.
14. CDC. 2008b. Outbreak of multidrug-resistant Salmonella enterica serotype Newport infections associated with consumption of unpasteurized Mexican-style aged cheese – Illinois, March 2006 – April 2007. MMWR Morb Mortal Wkly Rep 57:432-5.
15. CDC. 2008c. Outbreak of Listeria monocytogenes infections associated with pasteurized milk from a local dairy–Massachusetts, 2007. MMWR Morb Mortal Wkly Rep 57:1097-100.
16. CDC. 2009. Campylobacter jejuni Infection Associated with Unpasteurized Milk and Cheese — Kansas, 2007. MMWR Morb Mortal Wkly Rep 57:1377-9.
17. CDPH. 2008. Cluster of Campylobacter infections possibly associated with raw dairy products. Available at: http://www.marlerblog.com/Cluster%20of%20Campylobacter%20infections.pdf
18. CSPI. 2008. Outbreak Alert! 2008: Closing the gaps in our Federal food safety net. Available at: http://www.cspinet.org/new/pdf/outbreak_alert_2008_report_final.pdf
19. Dalton, C. B., C. C. Austin, J. Sobel, P. S. Hayes, W. F. Bibb, L. M. Graves, B. Swaminathan, M. E. Proctor, and P. M. Griffin. 1997. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med 336:100-5.
20. Fleming, D. W., S. L. Cochi, K. L. MacDonald, J. Brondum, P. S. Hayes, B. D. Plikaytis, M. B. Holmes, A. Audurier, C. V. Broome, and A. L. Reingold. 1985. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med 312:404-7.
21. Headrick, M. L., S. Korangy, N. H. Bean, F. J. Angulo, S. F. Altekruse, M. E. Potter, and K. C. Klontz. 1998. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health 88:1219-21.
22. Hennessy, T. W., C. W. Hedberg, L. Slutsker, K. E. White, J. M. Besser-Wiek, M. E. Moen, J. Feldman, W. W. Coleman, L. M. Edmonson, K. L. MacDonald, and M. T. Osterholm. 1996. A national outbreak of Salmonella enteritidis infections from ice cream. The Investigation Team. N Engl J Med 334:1281-6.
23. Jay M. T., J. Yuan, R. E. Mandrell, A. Bates, R. Manalac, J. O’Connell, J. Mohle-Boetani, W. G. Miller. 2007. Use of MOMP typing as an epidemiological tool during a large campylobacteriosis outbreak investigation. 107th General Meeting of the American Society for Microbiology, Toronto, Canada.
24. MacDonald, P. D., R. E. Whitwam, J. D. Boggs, J. N. MacCormack, K. L. Anderson, J. W. Reardon, J. R. Saah, L. M. Graves, S. B. Hunter, and J. Sobel. 2005. Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis 40:677-82.
25. Mazurek, J., E. Salehi, D. Propes, J. Holt, T. Bannerman, L. M. Nicholson, M. Bundesen, R. Duffy, and R. L. Moolenaar. 2004. A multistate outbreak of Salmonella enterica serotype typhimurium infection linked to raw milk consumption–Ohio, 2003. J Food Prot 67:2165-70.
26. Mead, P. S., L. Slutsker, V. Dietz, L. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-Related Illness and Death in the United States. Emerg Infect Dis 5:607-25.
27. Oliver, S. P., B. M. Jayarao, and R. A. Almeida. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog Dis 2:115-29.
28. Olsen, S. J., M. Ying, M. F. Davis, M. Deasy, B. Holland, L. Iampietro, C. M. Baysinger, F. Sassano, L. D. Polk, B. Gormley, M. J. Hung, K. Pilot, M. Orsini, S. Van Duyne, S. Rankin, C. Genese, E. A. Bresnitz, J. Smucker, M. Moll, and J. Sobel. 2004. Multidrug-resistant Salmonella Typhimurium infection from milk contaminated after pasteurization. Emerg Infect Dis 10:932-5.
29. Peterson, M. C. 2003. Campylobacter jejuni enteritis associated with consumption of raw milk. J Environ Health 65:20-1.
30. Ryan, C. A., M. K. Nickels, N. T. Hargrett-Bean, M. E. Potter, T. Endo, L. Mayer, C. W. Langkop, C. Gibson, R. C. McDonald, R. T. Kenney, and et al. 1987. Massive outbreak of antimicrobial-resistant salmonellosis traced to pasteurized milk. JAMA 258:3269-74.
31. Tacket, C. O., J. P. Narain, R. Sattin, J. P. Lofgren, C. Konigsberg, Jr., R. C. Rendtorff, A. Rausa, B. R. Davis, and M. L. Cohen. 1984. A multistate outbreak of infections caused by Yersinia enterocolitica transmitted by pasteurized milk. JAMA 251:483-6.