INVITED ARTICLE

FOOD SAFETY
Frederick J. Angulo, Section Editor

Unpasteurized Milk: A Continued Public Health Threat

Jeffrey T. LeJeune1,2 and Paivi J. Rajala-Schultz2
1
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Wooster, and 2Department of Veterinary Preventive Medicine,
College of Veterinary Medicine, Columbus, Ohio

Food available in the United States is plentiful, inexpensive,

and, for the most part, safe. Advances in animal production,
food processing and hygiene, and refrigeration have eliminated
several foodborne diseases that plagued Americans in the past
century. However, in the past 30 years, several previously unrecognized foodborne bacterial infections, including infection
with Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli strain O157, have emerged as significant causes of
human morbidity and mortality. Other infectious diseases once
believed to be controlled have started to reappear. It is estimated
that, each year, 76 million Americans become ill from eating
contaminated food [1].
Milk and other dairy products, primarily from cows but also
less frequently from goats and sheep, are important components of the American diet. The US Department of Agriculture
recommends that people consume 23 servings of dairy products daily. Inclusion of these products in the diet aides in the
prevention of certain diseases, such as obesity, hypertension,
Received 7 May 2008; accepted 16 September 2008; electronically published 3 December
2008.
Reprints or correspondence: Dr. Jeffrey T. LeJeune, Food Animal Health Research Program,
Ohio Agricultural Research and Development Center, 1680 Madison Ave., Wooster, OH 44691
([email protected]).
Clinical Infectious Diseases 2009; 48:93100
 2008 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2009/4801-0015$15.00
DOI: 10.1086/595007

and diabetes, and they are a source of calciumimportant for

growing bones and the prevention of osteoporosis [2]. In addition, dairy products also provide dietary sources of protein,
vitamins, and other minerals [3]. Notwithstanding the benefits,
there are some individuals who believe that milk is inappropriate for inclusion in the human diet [4]. Moreover, it has
long been recognized that milk is a vehicle for the transmission
of numerous bacteria of both human and animal origin. Milk
can be contaminated at any stage in the production-to-consumption continuum.
THE ORIGIN OF MILK CONTAMINATION
Commensal microflora. Typically, unless there is an intramammary infection or an animal has a systemic disease, milk
in the mammary gland at the site of its production does not
contain bacteria. However, as milk is excreted, it can become
contaminated with bacteria that live as commensal microflora
on the teat skin or on the epithelial lining of the teat canal,
the duct that conveys the milk from the mammary gland to
the teat orifice. In cattle, bacteria of the genera Staphylococcus,
Streptococcus, Bacillus, Micrococcus, and Corynebacterium and,
occasionally, coliforms colonize this location [5]. Thus, even
in a healthy animal, by the time the milk leaves the animal, it
may contain numerous bacterial contaminants.
Mastitis. The single disease that has the most significant
impact on milk quality is mastitis, the inflammation of the
FOOD SAFETY CID 2009:48 (1 January) 93

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Although milk and dairy products are important components of a healthy diet, if consumed unpasteurized, they also can
present a health hazard due to possible contamination with pathogenic bacteria. These bacteria can originate even from
clinically healthy animals from which milk is derived or from environmental contamination occurring during collection and
storage of milk. The decreased frequency of bovine carriage of certain zoonotic pathogens and improved milking hygiene
have contributed considerably to decreased contamination of milk but have not, and cannot, fully eliminate the risk of
milkborne disease. Pasteurization is the most effective method of enhancing the microbiological safety of milk. The consumption of milk that is not pasteurized increases the risk of contracting disease from a foodstuff that is otherwise very
nutritious and healthy. Despite concerns to the contrary, pasteurization does not change the nutritional value of milk.
Understanding the science behind this controversial and highly debated topic will provide public health care workers the
information needed to discern fact from fiction and will provide a tool to enhance communication with clients in an effort
to reduce the incidence of infections associated with the consumption of unpasteurized milk and dairy products.

94 CID 2009:48 (1 January) FOOD SAFETY

for C. jejuni, and 1.2% to 6.1% for Yersinia enterocolitica [21

24].
Moreover, the rich nutrient composition and neutral pH
make milk a good vehicle for the survival and growth of bacteria. Generally speaking, if milk is maintained properly chilled,
bacterial proliferation, with the exception of that of psychotropic organisms such as Listeria species, can be suppressed.
Unfortunately, prevention of proliferation is not sufficient to
ensure milk safetyeven low numbers of contaminating pathogens may be adequate to result in human illness. Thus, simple
survival of pathogens in milk is of major concern. Ultimately,
the nature and complex interaction among microflora initially
present in milk dictate how well pathogens will survive in milk
[2528].
In summary, there are 2 primary factors that contribute to
the microbiological quality of milk: the inclusion of organisms
in excreted milk (preharvest) and the contamination of milk
at the time of collection, processing, distribution, and storage
(postharvest). If pathogenic bacteria are among the contaminants, the product will pose a food safety threat. Several approaches have been used to minimize the possibility that milk
contaminated with pathogenic organisms will reach the consumer. These include enhanced animal health, improved milking hygiene, and pasteurization.
CONTAMINATION CONTROL STRATEGIES
An overwhelming majority of dairy producers feel responsible
for the safety and wholesomeness of the food products that
leave their farms [29]. Good animal health and hygienic conditions on the farm are important for the welfare of the animals
and the profitability of the producers, as well as for the quality
and wholesomeness of the raw food products leaving the farms
for human consumption. Nevertheless, many dairy producers
are unaware of the zoonotic potential of the most common
bacterial contaminants in milk. In a recent mail-based survey
of 461 Ohio dairy farm respondants, 36% did not think Salmonella species caused disease in humans. Likewise, 81%, 88%,
and 91% of farmers indicated that Listeria, Cryptosporidium,
and Campylobacter species, respectively, were not associated
with disease in humans (J.T.L., unpublished data).
Enhanced animal health. Over the past 100 years, veterinary care and diagnostic tests have improved, and many zoonotic diseases have been eliminated from the population of
food-producing animals in industrialized nations. On the other
hand, as mentioned above, there are a number of infections
that may be present in animals and remain completely asymptomatic yet have serious public health implications.
Improved milking hygiene. Complete control of microbiological hazards (i.e, zoonotic pathogens) is challenging, if
not impossible, in the dairy farm environment, because these
organisms may have multiple reservoirs; they do not always

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mammary gland. On the basis of bovine milk samples submitted to diagnostic laboratories during a period of several years
in New York and Pennsylvania (19911995) and Wisconsin
(19942001), the prevalence of intramammary infections was
50% [6, 7]. Staphylococcus and Streptococcus species were the
most commonly isolated bacteria from bovine milk in these
studies; 20% of the samples contained organisms of either
group. The milk produced by animals with subclinical mastitis
is not noticeably different from the milk produced by uninfected animals and frequently is added to the collection or
storage tank on a farm. Milk from cows with clinical mastitis,
however, typically has a changed appearance (i.e., it may contain flakes, clots, or blood or may have changed color) and is
withheld from human consumption.
Other diseases and environmental contamination.
Systemic disease can also result in localization of pathogens in
the mammary gland or associated lymph nodes and consequent
excretion of pathogens in milk. Bovine tuberculosis and brucellosis are classic examples of zoonotic milkborne diseases.
The contribution of cattle to the epidemiology of these 2 diseases in humans was so important that enormous efforts were
made to eradicate these infections among cattle in the United
States. The programs have largely been successful, and Mycobacterium bovis and Brucella abortus are seldom found in domestic US cattle [8].
In contrast to M. bovis and B. abortus, several other organisms are commonly found today in the milk of asymptomatic
US cattle and goats or contaminate milk from environmental
sources. These include Coxiella burnetii; Listeria species; Mycobacterium avium subspecies paratuberculosis; Campylobacter
species; coliforms, including E. coli; and Salmonella enterica [9
14]. Cattle can be a major reservoir of these organisms and
still remain clinically healthy and maintain near-optimal milk
production. For example, C. burnetii, the causal agent of Q
fever, is not an important cause of clinical disease in cattle;
however, its prevalence in pooled milk collected on farms in
the United States was reported to be 94%, on the basis of PCR
assays [15]. Similarly, a US Department of Agriculture 2007
dairy study estimated that at least 68% of all US dairy herds
are infected with M. avium subspecies paratuberculosis, the
causal agent of Johne disease, a chronic, progressive gastroenteritis of ruminants [16]. Although the association between
M. avium subspecies paratuberculosis and Crohn disease, a similar condition of humans, is debated, the zoonotic potential
exists [1719].
The dairy farm environment is an important reservoir for
many foodborne pathogens [20]. The frequency of contamination in pooled farm milk has been reported to be !1% to
8.9% for Salmonella species, 2.7% to 6.5% for L. monocytogenes,
!1% to 3.8% for Shiga toxinproducing E. coli, !1% to 12.3%

GUIDELINES, REGULATIONS, AND LAWS

RELATED TO MILK SAFETY AND
PASTEURIZATION
In the United States, the US Food and Drug Administration
(FDA), under the Department of Health and Human Services,
is responsible for providing oversight of quality standards for
dairy products and dairy processing. The milk sanitation program of the US Public Health Service is one of its oldest activities. In 1924, the US Public Health Servic developed a model
regulation known as the Standard Milk Ordinance for voluntary adoption by state and local milk-control agencies [31].
This regulation, known today as the Grade A Pasteurized
Milk Ordinance (PMO) was developed and is periodically reviewed and modified in cooperation with state and local governments, the dairy industry, and educational and research institutions. All 50 states have voluntarily adopted the PMO
guidelines. These guidelines provide guidance pertaining to all
aspects of production, handling, transportation, processing,
testing, and sale of milk. The guidelines are expected to minimize microbial contamination of milk and relate to areas such
as cow housing, milking barn hygiene, water supply, and sanitation methods. In addition, the PMO establishes maximum
allowable bacterial limits in raw milk destined for pasteurization, as well as in pasteurized milk. The federal government
and FDA, however, have no jurisdiction in the enforcement of
milk sanitation standards within state borders, and individual
states can establish regulations concerning adoption of specific
PMO recommendations and can decide on the rules regarding

Table 1. Time and temperatures for pasteurization of fluid milk

approved by the US Food and Drug Administration.
Temperature

Time, s

63C (145F)
72C (161F)

1800
15.0

89C (191F)
90C (194F)

1.0
0.5

94C (201F)
96C (204F)

0.1
0.05

100C (212F)

0.01

NOTE. Data are from [31].

the sale of unpasteurized milk within state borders. In 1987,

the FDA prohibited the interstate shipment of raw milk for
human consumption.
In 2006, the sale of raw milk was illegal in 26 states [32]. In
states where raw milk sales are not allowed, various schemes
have been developed to make raw milk available to the consumer. The marketing strategies designed to circumvent current
laws include selling raw milk labeled as animal or pet food
across state lines, publishing list of states where the sale of raw
milk is allowed, and selling shares in cows or leasing cows.
In buying shares of cows or leasing cows, consumers pay for
the upkeep, care, and milking of their cows (or portion thereof)
and, in return, receive raw milk from their animals, avoiding
the buying and selling of raw milk per se. In the states where
raw milk sales are legal, regulations varyin some states, the
sale of raw milk is allowed in retail outlets, whereas, in others,
it is restricted to on-farm sales directly to consumers, and the
volume of salable milk may be limited.
TRENDS IN CONSUMPTION OF RAW MILK
AND IN MILKBORNE DISEASES IN THE
UNITED STATES
Consumption of raw milk has always been common among
farm families, currently varying from 35% to 60% [21, 22, 24].
Most farm families report taste and convenience as the main
reasons for raw milk consumption [24]. A small portion of the
general US population also consumes raw milk. According to
the US Centers for Disease Control and Preventions FoodNet
Population Survey in 2002, 3.5% of respondents reported to
have consumed unpasteurized milk in the past 7 days before
the survey [33]. Demand for raw milk has considerably increased in recent years, despite the fact that public health officials consider the benefits of milk pasteurization to be undisputable. With the advent of mandatory pasteurization, the
incidence of milkborne diseases dropped dramatically. In the
United States in 1938, milkborne outbreaks constituted 25%
of all disease outbreaks due to contaminated food and water.
FOOD SAFETY CID 2009:48 (1 January) 95

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produce identifiable disease; their transmission pathways are

incompletely known; and cost-efficient, sensitive diagnostic
tests are not available. Dairy product food safety, however, can
be enhanced by implementing excellent hygienic standards for
housing and milking centers and cow cleanliness and through
uniform adoption of milking practices that reduce contamination of milk [30].
Pasteurization. Because of the above-mentioned challenges related to preharvest eradication of pathogens and the
ineffectiveness of environmental hygiene screening to adequately control microbial risks in milk, pasteurization has become the cornerstone of milk safety. Pasteurization is the process of heating milk for a predetermined time at a
predetermined temperature to destroy pathogens (table 1). The
current guidelines for temperature and time combinations for
pasteurization are based on the ability of the process to destroy
C. burnetii. The thermal destruction process is logarithmic, and
bacteria are killed at a rate that is proportional to the number
of bacteria present. Pasteurization improves the safety and
lengthens the shelf life of a product by destroying pathogenic
and spoilage organisms; however, it is not the same as
sterilization.

milk to consumers at the farm matched the outbreak strain

isolated from the case patients by PFGE. Sixteen of the 29 case
patients were aged !7 years [39]. At least 87 people became ill
in Kansas in 2 separate outbreaks of campylobacteriosis during
the end of 2007. In both outbreaks, illness was associated with
consumption of raw milk or raw-milk products [40]. In 2008,
an outbreak of campylobacteriosis in California was associated
with consumption of unpasteurized milk supplied from a farm
operating a cow-share program. One of the patients consequently developed Guillain-Barre syndrome [41]. Intrastate sale
of raw milk is legal in Washington, Pennsylvania, Kansas, and
California.
Opposition to pasteurization. Despite the overwhelming
scientific understanding of pathogens in milk and the public
health benefits of pasteurization, there is considerable disagreement between the medical community and raw-milk advocates
concerning the alleged benefits of consumption of raw milk
and the purported disadvantages of pasteurization. Raw-milk
advocates suggest that unpasteurized milk products are completely safe and that they can prevent and treat a wide spectrum
of diseases, including heart disease, kidney disease, cancer, and
lactose intolerance [4245]. In addition to the contaminating
microflora, milk contains substances that have bacteriostatic
and antimicrobial properties. The presumed role of these substances and their heat stability after exposure to pasteurization
temperatures are outlined in table 2. Scientific evidence to substantiate the assertions of the health benefits of unpasteurized
milk is generally lacking [57]. Nevertheless, when the public is
presented with a large body of conflicting information, their
decision-making process does not always yield the same results
as that of experts [58]. This problem is particularly complicated
by the fact that individuals with established attitudes not only
seek information that is supportive of their views [59, 60] but
also unconsciously process information in a biased fashion [61].

Figure 1. Reported outbreaks of disease suspected or confirmed to be associated with unpasteurized milk in the United States, 19932006. Data
are from [36].
96 CID 2009:48 (1 January) FOOD SAFETY

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At the beginning of the 21st century, milk and milk products

were associated with !1% of all such outbreaks [31].
Between 1880 and 1907, an average of 29 outbreaks of milkborne diseases were reported each year in the United States
[34]. Headrick et al. [35] reported 46 outbreaks of milkborne
disease in the 19-year period from 19731992; an average of
2.4 per year. A review of foodborne diseases reported to the
CDC [36] that were suspected or confirmed to be associated
with unpasteurized milk or milk products between 19932006
identified 68 outbreaks, an average of 5.2 per year (figure 1).
Although some of this increase may be a result of increased
detection and reporting, it is clear that disease associated with
the consumption of raw milk is still an important public health
concern in the United States. Very young, aged, infirm, or
immunocompromised persons are the most susceptible to the
pathogens that may be present in raw milk. However, anyone
can be affected, including healthy young adults, as described
by Blaser et al. [37] in an outbreak of C. jejuni infection among
19 of 31 college students who consumed unpasteurized milk
on a vist to a farm.
Recent disease outbreaks related to consumption of raw
milk. Since 2005, several outbreaks of disease, including salmonellosis, campylobacteriosis, and E. coli O157:H7 infection,
that were related to consumption of unpasteurized milk or
dairy products have been reported. During the end of 2005,
18 cases of infection with E. coli O157:H7, mostly among children aged !14 years, occurred in Oregon and Washington
states. Five patients, aged 113 years, were hospitalized, 4 with
hemolytic uremic syndrome. Laboratory and risk factor analyses linked the cases to raw milk from a dairy participating in
a cow-share program in Washington [38]. In 2007, 29 cases of
S. enterica serotype Typhimurium infection were associated with
consumption of raw milk or raw-milk products in Pennsylvania. A S. typhimurium strain isolated from a dairy selling raw

Transfers immunity to bovine pathogens to calves; may provide

some lactogenic immunity in the gut
A primary sugar present in milk

Bovine immunoglobulin

Lactose

Xanthine oxidase

Oligosaccharides

Bacteriocins

Vitamin C

Vitamins

Pasteurization does not change the concentration of lactose but

will destroy lactase-producing bacteria that might be present
and that might aid in the tolerance to dairy products among lactase-deficient persons. With heating, lactose in milk is degraded
initially into lactulose and epilactose and subsequently into galactose and tagatose. Large doses of indigestible carbohydrates,
including lactulose, may cause digestive upset in lactose maldigestors. However, pasteurization does not typically lead to detectable levels of lactulose present in milk.
The nutritive value of these proteins is largely unaffected by
pasteurization

An enzyme linked with flavor; changes in milk during storage

Have narrow-spectrum antimicrobial activity; often produced by

other bacteria contaminating milk
Competitively bind to pathogens to prevent adherence of pathogens to target mucosal receptors

[55]
[56]

Retains enzymatic activity after 7 min at 73C, or 50 s at 80C

[53, 54]

[48]

[52]

[50, 51]

[49]

[48]

[47]

Heat stable

Heat-stable; retain activity after pasteurization

Milk is a good source of the B-complex vitamins thiamine, folate, Pasteurization does not cause appreciable losses of the fat-soluble
and riboflavin
vitamins A, D, E, and K
Milk contains a small amount of vitamin C, but it is not considered Pasteurization will result in a loss of 0%10% of the vitamin C
to be a good dietary source of it
present

Other milk proteins (caseins, Render milk more allergenic; studies show that the sensitizing cawhey, and others)
pacity of cows milk is retained or, usually, reduced after heat
treatment, whereas pasteurization minimizes the heat destruction of nutrients

In conjunction with lactoferrin, has bactericidal effects

Lysozyme

In excess of 75% of bovine milk, lysozyme will survive at 80C for

15 s
No loss in activity when held for 30 min at 62.7C; retains
59%76% of activity after high-temperature, short-time
pasteurization

A milk enzyme, which, in conjunction with other enzymes, contrib- Retains 70% activity when heated to 72C for 15 s, with further
utes to the bacteriostatic properties of milk. To be effective,
decreases in activity as the temperature is increased
both hydrogen peroxide and thiocyanate ions must be present;
both of these chemicals are not endogenous to milk but are byproducts of other bacterial metabolic activity.

[46]

Unheated and pasteurized bovine lactoferrin have similar antibacterial properties; ultrahigh-temperature treatment denatures the
protein

Lactoperoxidase

Reference(s)

Effects of pasteurization

An iron-binding protein; scavenger of iron, thereby providing antibacterial effects by limiting the availability of free iron required
for bacterial proliferation

Role in milk

Lactoferrin

Nutrient

Table 2. Effects of pasteurization on proteins and other milk components.

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SUMMARY AND CONCLUSIONS

Despite the enormous advances in animal health, milking hygiene, and processing technology that have occurred during the
past century, milkborne disease outbreaks continue to occur in
the United States. Given that milk is derived from animals, it
inherently carries the risk of being contaminated with pathogens from its source (cattle, goats, sheep, and the farm environment). The key factor in the prevention of milkborne disease
is consumer avoidance of raw milk consumption. In an effort
to protect human health, a number of organizations have published guidelines and statements concerning milk pasteurization. The American Medical Association (policy H-150.980)
[67] clearly asserts that milk sold for human consumption
should be pasteurized. Likewise, the American Veterinary Medical Association asserts that only pasteurized milk and milk
products should be sold for human consumption [68]. Thus,
physicians, veterinarians, and dairy farmers who promote, or
even condone, the human consumption of unpasteurized milk
and dairy products may be at risk for subsequent legal action
[32, 69].
98 CID 2009:48 (1 January) FOOD SAFETY

Acknowledgments
The authors thank Dr. John Sheehan for valuable discussions on the
subject during the preparation of the manuscript.
Financial support. Funding in partial support of J.T.L. was provided
by state and federal funds allocated to the Ohio Agricultural Research and
Development Center, Wooster, Ohio.
Potential conflicts of interest. J.T.L. and P.J.R.-S.: no conflicts.

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in a product, (3) extremely small amounts are infectious, and
(4) extremely small numbers (below the detectable limit) of
organisms present in the product may proliferate to levels that
reach unacceptable risks after testing.

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