Nonpasteurized Dairy Products, Disease Outbreaks, and State Laws—United States, 1993–2006

Most dairy-associated outbreaks occurred in states that permitted sale of these products.

I n the United States, milk and other dairy products are dietary staples; the 2010 Dietary Guidelines for Americans recommend that most Americans include dairy products in their diet (1). However, numerous pathogens can contaminate dairy products and cause illness and death. Milkborne infections were relatively common before the advent of pasteurization in the late 19th century (2), and in the United States today, illness related to consumption of nonpasteurized dairy products remains a public health problem.
In 1948, Michigan enacted the fi rst statewide requirement that dairy products be pasteurized, and many other states soon did the same (2). In 1987, the United States Food and Drug Administration prohibited distribution of nonpasteurized dairy products in interstate commerce for sale to consumers (3). However, sale of nonpasteurized dairy products within the state where they are produced is regulated by each state, and some states permit sale of these products. Despite the federal ban on the sale of nonpasteurized products in interstate commerce, the broad use of pasteurization by the dairy industry, and the infrequency with which nonpasteurized dairy products are consumed, illnesses and outbreaks associated with consumption of these products continue to occur (4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).
State and local health departments report foodborne disease outbreaks to the Centers for Disease Control and Prevention (CDC) through the Foodborne Disease Outbreak Surveillance System. As a result of efforts to enhance outbreak surveillance starting in 1998, the total number of outbreak reports increased substantially (24). A recent comprehensive analysis of foodborne disease outbreaks associated with dairy products (dairy-associated outbreaks) reported to CDC reviewed outbreaks that occurred during 1973-1992 (4). We reviewed subsequent dairy-associated outbreaks, reported in the United States during 1993-2006. We characterized the outbreaks and examined their association with state laws regarding sale of nonpasteurized dairy products.

Methods
To compare the incidence of foodborne outbreaks involving nonpasteurized dairy products among states with differing laws with regard to the sale of these products (i.e., states that permitted their sale vs. states that prohibited their sale), we reviewed reports of foodborne disease outbreaks involving dairy products reported to CDC during 1993-2006. These reports, completed by state and local health departments, typically included the number of cases associated with the outbreak; the age and sex distribution of outbreak-associated case-patients; the number of hospitalizations and deaths; the etiologic agent associated with the outbreak; the type of dairy product implicated (e.g., fl uid milk, cheese); and whether the implicated dairy product was marketed, labeled, or otherwise presented to the consumer as pasteurized or nonpasteurized. Hereafter, we refer to these products as pasteurized or nonpasteurized. Thus, any outbreak involving a dairy product that was contaminated after pasteurization or that was intended to be pasteurized but underwent inadequate pasteurization was classifi ed as involving pasteurized product. When possible, we corrected missing or incomplete data by asking the health department that conducted the investigation for more information.
To determine whether the sale of nonpasteurized dairy products was legal at the time of each outbreak, we contacted the 50 state departments of health and agriculture and requested data on whether the state permitted the sale of nonpasteurized dairy products produced in that state for each year from 1993 through 2006. We defi ned an illegal state-year as a year in which a state prohibited the sale of all nonpasteurized products, and we defi ned a legal state-year as a year in which a state permitted the sale of nonpasteurized dairy products produced in that state. Data on the estimated population, by state, for each year were obtained from the US Census Bureau. To compare the incidence of outbreak and outbreak-associated cases during illegal state-years to that during legal state-years, we stratifi ed the outbreaks by legal status of the state in which the outbreak occurred at the time of the outbreak and calculated incidence density ratios for reported outbreaks (Poisson model) and for outbreak-associated cases (zeroinfl ated negative binomial model).

Results
During 1993-2006, a total of 30 states reported 122 foodborne disease outbreaks caused by contaminated dairy products. Dairy-associated outbreaks occurred in all years except 1996, and outbreaks involving nonpasteurized dairy products occurred in all years except 1994 and 1996. The number of reported dairy-associated outbreaks increased in 1998 after surveillance for foodborne disease outbreaks was enhanced (Figure 1).
Whether the product was pasteurized or nonpasteurized was known for 121 of the 122 outbreaks, and most outbreaks (73 [60%]) involved nonpasteurized dairy products. Of the 121 outbreaks for which product pasteurization status was known, 65 (54%) involved cheese and 56 (46%) involved fl uid milk.
Of the 65 outbreaks involving cheese, 27 (42%) involved cheese made from nonpasteurized milk. Of the 56 outbreaks involving fl uid milk, an even higher percentage (82%) involved nonpasteurized milk.
The 121 outbreaks involving dairy products for which pasteurization status was known resulted in 4,413 reported illnesses. Among these illnesses, 1,571 (36%) resulted from nonpasteurized dairy products. The median number of persons reported ill during outbreaks involving nonpasteurized dairy products was 11 (range 2-202). Outbreaks involving nonpasteurized dairy products resulted in 202 hospitalizations (hospitalization rate 13%). In contrast, outbreaks involving pasteurized dairy products resulted in 37 hospitalizations (hospitalization rate 1%). Two deaths were associated with an outbreak caused by consuming nonpasteurized dairy products, and 1 death was associated with an outbreak caused by a pasteurized product (Table).
Ill persons in outbreaks involving nonpasteurized dairy products were generally younger than those in outbreaks involving pasteurized dairy products. For the 60 outbreaks involving nonpasteurized dairy products for which age of patients was known, 60% of patients were <20 years of age; for the 37 outbreaks involving pasteurized dairy products for which age of patients was known, 23% of patients were <20 years of age (p<0.001).
A total of 48 reported outbreaks involved pasteurized dairy products. The source of contamination was reported for 7 (14%) of these outbreaks, of which at least 4 (57%) probably resulted from post-pasteurization contamination by an infected food handler. Failure of the consumer to store the dairy product at an appropriate temperature probably contributed to 3 other outbreaks. Such temperature abuse can enable pathogens (present because they either survived pasteurization in low numbers or were introduced after pasteurization) to multiply to concentrations capable of causing illness.
During the study period, 43 (86%) states did not change their legal status regarding the sale of nonpasteurized dairy products produced in that state. Among these 43 states, selling nonpasteurized dairy products produced in that state was legal in 21 (49%). Of the 7 states that changed their legal status, 3  Among the 700 state-years (14 years × 50 states) included in our analysis of the association of legal sales status and nonpasteurized dairy-associated outbreaks, sale of nonpasteurized dairy products produced in the state was legal for 342 state-years and illegal for 358 stateyears. We excluded from analysis 2 outbreaks caused by nonpasteurized dairy products because each occurred in multiple states with differing laws. Of the 71 remaining outbreaks involving nonpasteurized dairy products, 55 (77%) occurred in states where sale of nonpasteurized dairy products produced in that state was legal. Among these 71 outbreaks involving nonpasteurized dairy products, 1,526 persons became ill and 1,112 (73%) of these illnesses occurred in states where it was legal to sell nonpasteurized dairy products. Also among these 71 outbreaks involving nonpasteurized dairy products, 15 occurred in states where sale of nonpasteurized dairy  products was illegal. The source of the nonpasteurized dairy products was reported for 9 of these outbreaks: 7 (78%) were associated with nonpasteurized dairy products obtained directly from the producing dairy farm, 1 was associated with nonpasteurized dairy products obtained under a communal program to purchase shares in dairy cows (i.e., cow shares, a scheme used to circumvent state restrictions on commercial sales of nonpasteurized dairy products) (11), and 1 was limited to members of a large extended family who consumed nonpasteurized milk from their own cow.
Incidence density ratios (IDRs) for nonpasteurized product-associated outbreaks and outbreak-associated cases during legal and illegal state-years varied by the type of dairy product (milk or cheese) and are reported separately. In states where it was legal to sell nonpasteurized dairy products, the rate of outbreaks caused by nonpasteurized fl uid milk was >2× as high as in states where it was illegal to sell nonpasteurized dairy products (IDR 2.20, 95% CI 1.14-4.25). The rate of outbreak-associated illnesses caused by nonpasteurized fl uid milk was 15% higher in states where it was legal to sell nonpasteurized dairy products, but this result was not statistically signifi cant (IDR 1.15, 95% CI 0.24-5.54). States where it was legal to sell nonpasteurized dairy products had nearly 6× the rate of outbreaks caused by cheese made from nonpasteurized milk (IDR 5.70, 95% CI 1.71-19.05) and nearly 6× the rate of outbreak-associated illnesses (IDR 5.77, 95% CI 0.59-56.31), although the IDR for outbreak-associated illnesses was not statistically signifi cant.

Discussion
Incidence of outbreaks caused by nonpasteurized dairy products was higher in states that permitted the sale of nonpasteurized dairy products than in states that prohibited such sale. This association was evident for nonpasteurized fl uid milk and cheese made from nonpasteurized milk. Although this association did not extend to the rates of outbreak-associated cases, factors other than whether it was legal to sell nonpasteurized dairy products probably affect the number of cases that occur in an outbreak. These factors include the volume and area of distribution of the contaminated product, the pathogen involved, the underlying health status of the exposed persons, and the ability of the responding public health agency to swiftly intervene to terminate the outbreak.
Because consumption of nonpasteurized dairy products is uncommon in the United States, the high incidence of outbreaks and outbreak-associated illness involving nonpasteurized dairy products is remarkable and greatly disproportionate to the incidence involving dairy products that were marketed, labeled, or otherwise presented as pasteurized. In a population-based survey conducted in 1996-1997, only 1.5% of respondents reported having consumed nonpasteurized dairy products in the 7 days before being interviewed; and in the 2003-2004 and 2005-2006 National Health and Nutrition Examination Surveys, only <1% of respondents who drank milk reported that they usually drank nonpasteurized milk (21,25,26). Because many of these respondents also reported consuming pasteurized dairy products, the proportion of dairy products consumed nonpasteurized by volume or weight is probably <1%. To illustrate this point, it is useful if we provide a hypothetical weighting of the fi ndings in this study by the  (27). If 1% of dairy products were consumed nonpasteurized, then during these 14 years, 73 outbreaks were caused by the 27 billion pounds of nonpasteurized dairy products that were consumed and 48 by the 2,673 billion pounds of pasteurized products that were consumed. Therefore, the incidence of reported outbreaks involving nonpasteurized dairy products was ≈150× greater, per unit of dairy product consumed, than the incidence involving pasteurized products. If, as is probably more likely, <1% of dairy products are consumed nonpasteurized, then the relative risk per unit of nonpasteurized dairy product consumed would be even higher.
After 1998, when surveillance for foodborne outbreaks was enhanced, the number of reported foodborne disease outbreaks caused by dairy products increased, as did the total number of reported foodborne outbreaks. Outbreaks involving nonpasteurized dairy products were all associated with bacterial enteric pathogens, most of which have known animal reservoirs. In contrast, among outbreaks in which a pasteurized dairy product was implicated, the most commonly reported causative agent was norovirus (44% of outbreaks), a pathogen with a human reservoir. These results suggest that outbreaks caused by nonpasteurized dairy products are probably caused by pathogens in the dairy environment, which would be eliminated by proper pasteurization, and that outbreaks caused by pasteurized dairy products are probably caused by contamination of the products at some point after pasteurization.
The objective of pasteurization is to eliminate from fl uid milk those pathogens that originate in the dairy environment; however, pasteurization does not protect against contamination that might occur later, such as during food handling. In addition, if pasteurization is not performed properly (for appropriate times and at appropriate temperatures), pathogens might not be eliminated from the milk. Appropriate post-pasteurization food-handling practices can minimize the risk for reintroduction of pathogens into dairy products after pasteurization. In addition, other precautions, such as maintaining the dairy product at an appropriate temperature and disposing of expired products, reduce the risk to the consumer should the product become contaminated after pasteurization. When outbreaks do occur because of contamination of dairy products that are marketed as pasteurized, the source of contamination is typically traced to improper pasteurization, improper storage, or improper handling of the products after marketing (28)(29)(30). In our study, all outbreaks associated with pasteurized products for which information on the source of contamination was available were attributed to post-pasteurization mishandling.
Among outbreak-associated cases involving nonpasteurized dairy products, 60% involved persons <20 years of age. Public health and regulatory authorities are obligated to protect persons who cannot make fully informed decisions (e.g., children) from potential health hazards. Dietary decisions for younger children, in particular, are often made by caregivers. The American Academy of Pediatrics advises against giving nonpasteurized dairy products to children and recommends that pediatricians counsel caregivers against use of these products (31).
Proportionately more persons were hospitalized during outbreaks caused by nonpasteurized (13%) than by pasteurized dairy products (1%). This observation suggests that infections associated with nonpasteurized dairy products might be more severe, and it is consistent with the more frequent identifi cation of bacterial, rather than viral or toxic, causative agents and with the larger proportion of illnesses affecting children.
Limitations of this analysis are primarily associated with the nature of the CDC Foodborne Disease Outbreak Surveillance System. Outbreak reporting by state and local health departments is voluntary, and outbreak reports are not always complete. For this analysis, we obtained missing data whenever possible by contacting the reporting state health department. In addition, the CDC outbreak surveillance database is dynamic; reporting agencies can submit new reports and can change or delete previous reports at any time as new information becomes available. Therefore, the results of this analysis represent data available at 1 point in time and might differ from those published earlier or subsequently.
In summary, foodborne outbreaks involving dairy products continue to be a public health problem in the United States, and this problem is disproportionately attributable to nonpasteurized dairy products. Since the US Food and Drug Administration prohibited distribution of nonpasteurized dairy products in interstate commerce for sale to consumers in 1987, all legal sale and distribution has occurred within states that permit the sale of nonpasteurized dairy products that originated in that state. How much illegal distribution in interstate commerce continues is unknown. The increased risk for outbreaks associated with legal intrastate sale of nonpasteurized dairy products demonstrated in this analysis can be weighed against the purported nutritional or other health benefi ts attributed to these products. Scientifi cally credible evidence for the health benefi ts of nonpasteurized dairy products beyond the benefi ts of those of otherwise equivalent pasteurized products is lacking (32). The risk for outbreaks resulting from cheese made from nonpasteurized milk in states where nonpasteurized milk sale is legal may be higher for particular groups within those states. For example, in recent years, foodborne outbreaks involving nonpasteurized dairy products have been reported in association with traditional nonpasteurized products marketed to the growing Hispanic community in the United States (5,33).
Our analysis shows that legal intrastate sale of nonpasteurized dairy products is associated with a higher risk for dairy-related outbreaks and implies that restricting sale of nonpasteurized dairy products reduces the risk for dairy-related outbreaks within that state. Pasteurization is the most reliable and feasible way to render dairy products safe for consumption. Although warning labels and signs or government-issued permits are prudent where the sale of nonpasteurized dairy products is legal, they have not been shown to be effective and, given the results of this analysis, do not seem to reduce the incidence of outbreaks involving nonpasteurized dairy products to the degree that pasteurization does (18). Whether certain types of warnings or more explicit health advisories might be more effective than others is unknown. Public health offi cials at all levels should continue to develop innovative methods to educate consumers and caregivers about the dangers associated with nonpasteurized dairy products. State offi cials should consider further restricting or prohibiting the sale or distribution of nonpasteurized dairy products within their states. Federal and state regulators should continue to enforce existing regulations to prevent distribution of nonpasteurized dairy products to consumers. Consumption of nonpasteurized dairy products cannot be considered safe under any circumstances.