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7
Scientific Criteria and
Performance Standards to Control Hazards
in Dairy Products
High morbidity and mortality rates associated with diseases such as typhoid
fever and infantile diarrhea, which may be contracted through consumption of
microbiologically contaminated foods, led to initiation of food- and water-borne
disease reporting in the United States more than 75 years ago (Olsen et al., 2000~.
Anecdotal observations that linked consumption of milk with the spread of dis-
ease spurred various scientists and physicians in the United States and around the
world to undertake public health research to investigate the role of milk con-
sumption in foodborne disease as early as the turn of the twentieth century. As a
result of these investigations, consumption of unpasteurized milk was found to be
associated with many serious diseases, including diphtheria, typhoid, tuberculo-
sis, and brucellosis (Johnson et al., 1990~.
The first reports of gastrointestinal disease outbreaks attributed to milk con-
sumption were published by the Public Health Service (PHS) in 1925. These
early reports provided evidence suggesting that to control milk-borne diseases,
sanitation measures would need to be applied at all points in the food system,
from the farm to the consumer (CFSAN,2002~. Further, these observations high-
lighted the need for technical research that would determine the bacterial destruc-
tion characteristics of food-processing treatments for pathogenic microbes likely
to be present in raw milk (Enright et al., 1957; Gilman et al., 1946~. The results of
these studies led to the development of specific recommendations for pasteuriza-
tion and other intervention strategies (described below) that were designed to
protect the public from exposure to hazardous microorganisms that may be present
in raw milk. In the case of cheese, however, investigations were initiated not
because of the association between illness and cheeses made from unpasteurized
225
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226
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
TABLE 7.1 Equivalent Temperature and Time Combinations for Milk
Pasteurization According to U.S. Regulations
Temperature Time Temperature Time
63°C (145°F)a 30 men 94°C (201 °F) 0.1 see
72°C (161°F)a 15 sec 96°C (204°F) 0.05 sec
89°C (191°F) 1.0 see 100°C (212°F) 0.01 see
90°C (194°F) 0.5 see
a If the fat content of the milk is 10% or more, or if it contains added sweeteners, the required
minimum temperature must be increased by at least 3°C (5°F).
SOURCE: CFSAN (2002).
milk, but to assess the survival of Brucella abortus in the product (Gilman et al.,
1946~. In the past few decades, foodborne disease outbreaks have been linked to
various cheeses and, therefore, the need to evaluate the survival of human patho-
gens during cheese manufacturing and aging has been revisited. In light of data
indicating that certain pathogens (Listeria monocytogenes and Escherichia cold
0157:H7) may survive the 60-day aging period in cheese, research is currently
being conducted to determine if this process criterion is adequate to protect
public health.
For the purpose of this report, "raw milk" is defined as milk, harvested from
an animal, that may have been cooled to refrigeration temperatures or below, but
that has not been subjected to processing with the objective of eliminating patho-
genic bacteria that may be present. "Unpasteurized milk" is milk that may have
been cooled or heated, but that has not been subjected to the minimal pasteuriza-
tion processing conditions described in Table 7.1. While these terms are typically
used interchangeably, unpasteurized milk is a broader term than raw milk as, for
example, milk that can be processed into some types of cheeses may be subjected
to heat treatments below minimum pasteurization conditions. Milk treated in this
manner would be considered unpasteurized but not raw. (For a full discussion of
the use of unpasteurized milk in dairy-product manufacturing, see later section,
"Cheese and Other Dairy Food Products.")
MILK
Current Criteria and Standards
PHS implemented the Standard Milk Ordinance in 1924 to assist states and
cities in the voluntary adoption of programs designed to control milk-borne dis-
ease. In 1950, the U.S. Surgeon General invited state milk-sanitation regulatory
agencies to establish procedures for a voluntary Interstate Milk Shipper Certifica-
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
227
tion Program, which resulted in the formation of the National Conference on
Interstate Milk Shipments (NCIMS) and the Cooperative State-Public Health
Service Program for the certification of interstate milk shippers (CFSAN, 2000~.
Responsibilities under this program were divided between state agencies and
PHS. In 1969, the PHS responsibilities were transferred to the Food and Drug
Administration (FDA). Currently, all states, the District of Columbia, and the
United States trust territories participate in NCIMS.
PHS, and later FDA, recommended the application of the current Grade A
Pasteurized Milk Ordinance, commonly referred to as the PMO (CFSAN, 2002),
to provide national uniformity for milk sanitation standards. Milk products covered
by the PMO include products such as creams, concentrated milks, yogurts, and
low-fat and skim milks (CFSAN,2002~. FDA's Division of Dairy and Egg Safety,
Office of Plant and Dairy Foods and Beverages, is responsible for the develop-
ment of additional regulations to protect the safety of cheese and other dairy
foods (infant formula, dried milk products, ice cream or other frozen desserts,
butter, and cheese) that enter interstate commerce, but that are not specifically
covered by the PMO.
The PMO covers production, transportation, processing, handling, sampling,
examination, labeling, and sale of milk and milk products; the inspection of dairy
farms and milk plants; the issuing and revocation of permits to milk producers,
haulers, and distributors; and the fixing of penalties (CFSAN,2002~. The PMO is
considered the reference for federal specifications for the procurement of milk
and dairy products and as the sanitary regulation for dairy products served during
interstate travel. It is also recognized by public health agencies and the dairy
industry as the national standard for milk sanitation. As knowledge and experi-
ence is gained, modifications to the PMO are recommended during biennial
NCIMS meetings, which then must be approved by FDA before incorporation
into the PMO. Since 1924, the PMO has evolved with input from many sources,
including federal, state, and local government health and agriculture departments,
the dairy industry (from producers to associations), academic organizations, and
individuals. Hence, the PMO is derived from broad-based consensus of current
knowledge and experience with milk sanitation standards in the United States.
The implementation and enforcement of the PMO is another key element to
protect the public from milk-borne illness. In this regard, FDA has no legal
jurisdiction to enforce milk sanitation standards, except for interstate carriers and
for products in interstate commerce.
In general, although state and local agencies bear the majority of enforce-
ment responsibilities for dairy regulatory programs, they still commonly use the
PMO as the basis for developing their programs. Since 1924, government,
academia, and industry have worked together to address targeted research needs
as new pathogens have been identified and to modify regulations when science-
based research has revealed appropriate measures for destruction and control of
microbiological hazards.
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SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
The development, implementation, and enforcement of the PMO provide a
good model for an integrated "cow-to-cup" strategy for product safety assurance.
In addition, this model also provides a specific structure and mechanism for
biennial review of existing regulations directed toward the fluid milk industry.
Although FDA has the authority to enforce the implementation of the PMO
standards in milk for interstate commerce, milk for local consumption is not
subject to FDA oversight. Therefore, consumption of unpasteurized or raw milk
continues to be an issue of concern, since it has been clearly established as a high-
risk behavior for contracting foodborne illness.
The committee concludes that targeted educational programs that illustrate
the hazards of raw milk and raw milk-product consumption for milk producers
and for the general public are warranted.
The Public Health Objective of Fluid Milk Processing
The public health objective for milk pasteurization, as defined in the PMO, is
to eliminate all nonspore-forming pathogens commonly associated with milk;
nevertheless, the guidance document cautions that pasteurization may not destroy
preformed toxins (CFSAN, 2002~.
According to the PMO, an analysis of milk-borne outbreak data over the
years indicates that the risk of contracting disease is about 50 times less when
consuming pasteurized versus unpasteurized milk. Pasteurization, as first adopted
in the United States, was defined in the 1939 Milk Ordinance and Code as "the
process of heating every particle of milk to at least 143°F (61.7°C) and holding at
such temperature for at least 30 minutes, or to at least 160°F (71.1 °C) and holding
at such temperature for at least 15 seconds, in approved and properly operated
equipment" (PHS, 1940~. These heat treatments were referred to as the "holding
method" or vat/batch pasteurization, and the "flash method" or high-temperature,
short-time pasteurization, respectively. Table 7.1 contains these and other equiva-
lent temperature/time combinations allowed by U.S. regulations.
To address recognized scientific gaps regarding knowledge of the microbes
associated with milk-borne disease, extensive research was conducted to deter-
mine the heat treatment required to kill Mycobacterium tuberculosis which, at the
time, was considered to be the most heat-resistant pathogen associated with milk
(Hammer, 1948~. This work led to the widespread recognition of the public
health significance of thermal milk processing and formed the basis for modern
pasteurization processes (Hammer, 1948~. In 1956, minimal pasteurization tem-
peratures were slightly increased to those listed in Table 7.1 to assure destruction
of Coxiella burnetti, the organism associated with Q fever, which was found to be
more heat resistant than M. tuberculosis (Enright et al., 1957~.
As described above, the PMO prescribes highly specific pasteurization con-
ditions (i.e., time and temperature combinations), equivalent to process standards,
to ensure the safety of dairy products.
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
The Scientific Basis for Current Pasteurization Requirements
229
The observation of a significant number of cases of Q fever attributed to the
consumption of raw milk in the United States in the 1940s and 1950s inspired
targeted research to precisely define conditions required for thermal destruction
of C. burnetti (Enright et al., 1957~. Q fever, which was first described in the mid-
1930s, is a rickettsial disease characterized by chills, fever, weakness, and head-
ache, with endocarditis as a possible complication in immunocompromised
patients. C. burnetti is an obligate intracellular parasite that cannot multiply
outside of living host cells; therefore, it cannot be cultured in laboratory media.
While new detection strategies (e.g., polymerase chain reaction-based methods)
are under development, current diagnostic strategies for Q fever are still based on
the measurement of antibody titers for C. burnetti in blood samples taken from
patients. High numbers of C. burnetti-specific antibodies in a patient's blood are
considered to be indicative of exposure to this organism.
Experiments to ascertain the thermal destruction of C. burnetti are techni-
cally challenging because the presence of this organism in a heat-treated milk
sample can only be measured indirectly by assessing the presence and concentra-
tion of antibodies in a host animal that has been inoculated with a sample of the
milk. Current milk processing strategies, which are designed to destroy C. burnetti
in raw milk, are the outcome of a collaborative project between PHS and the
University of California in the mid-1950s. The objectives of this study were to
determine the maximum number of C. burnetti that might be found in the milk of
an infected cow, to develop a sensitive method for determining the presence of
small numbers of C. burnetti in pasteurized milk, and to ascertain the thermal
resistance of C. burnetti in whole raw milk to ensure the absence of viable
organisms in processed milk products (Enright et al., 1957~. The guinea pig was
the host animal selected for monitoring residual levels of C. burnetti in heat-
treated milk samples. Numbers of C. burnetti present in the milk were referred to
as "infective guinea pig doses" because they were assessed through a determina-
tion of the highest tenfold milk dilution that caused an intraperitoneally inocu-
lated guinea pig to have a significant rise (at least fourfold) in antibody titer to
C. burnetti (Enright et al., 1957~. The highest level of C. burnetti in milk of
infected cows from samples collected around the state of California was deter-
mined to be 10,000 infective guinea pig doses. Therefore, to provide an additional
margin of safety, the authors selected thermal destruction of 100,000 infective
guinea pig doses as the goal for minimal pasteurization conditions (Enright et al.,
1957~. For the purpose of contrasting this thermal processing goal with other
microbial destruction strategies described in this report, destruction of 100,000
infective guinea pig doses would be equivalent to a 5-D reduction in infective
capacity for a given volume of milk. The pasteurization conditions described in
Table 7.1 were found to result in destruction of 100,000 infective guinea pig
doses of C. burnetti. Therefore, on July 16, 1956, the U.S. Assistant Surgeon
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230
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
General released a recommendation for a minimum raw milk heat treatment of
145°F for 30 min or 161°F for 15 sec to ensure protection of the public from
exposure to C. burnetti through consumption of milk. While the results reported
by Enright and colleagues (1957) still serve as the scientific basis for current milk
pasteurization practices, many processors apply time and temperature combina-
tions that are above the minimum conditions (Douglas et al., 2000~.
As discussed in Chapter 3 and mentioned in Chapters 4 and 5, the committee
reiterates its belief that the implementation of performance standards that specify
the reduction in numbers required for a targeted organism (e.g., a 5-D reduction
for infective guinea pig doses for C. burnetti) in a food product (milk in this
case), rather than specifying the precise conditions (i.e., process standards) for
achieving that end, as currently practiced, could enable greater flexibility and
innovation in the dairy industry, perhaps enabling the adoption of effective new
processing technologies.
Emerging Food Safety Concerns That May Justify a Reexamination of
Current Milk Pasteurization Conditions
As mentioned previously, currently applied thermal processing conditions
for Grade A raw milk are designed to destroy the most heat-resistant of currently
recognized nonspore-forming human pathogens, namely C. burnetti. However,
some microbes that may be present in raw milk can survive pasteurization
(Hammer et al., 1995~. Spore-forming bacteria, including those of the Bacillus
and Clostridium genera, are among the heat resistant organisms that can be iso-
lated from pasteurized milk. While the public health risk associated with the
presence of these organisms in processed milk products is considered insignifi-
cant under the current PMO, it is very important to recognize the fact that the
pasteurization process is not intended to sterilize raw milk.
In addition to incomplete destruction of spore-forming bacteria, the efficacy
of milk pasteurization in killing M. avium subspp. paratuberculosis, a bacterium
that causes Johne's disease in cattle but that has not been proven to cause
human disease is uncertain (Klijn et al., 2001; Mechor, 1997~. Furthermore,
although no evidence exists linking development of encephalopathy to con-
sumption of milk from cows infected with bovine spongiform encephalopathy
(commonly referred to as mad cow disease), current pasteurization conditions do
not inactivate the causative prion. This prion, an infectious protein, shows little
loss of infectivity even after prolonged exposure to temperatures up to 176°F
(80°C) (Asher et al., 1986~. Although mice injected with milk from bovine
spongiform encephalopathy-infected cattle did not develop the disease nor have
epidemiological analyses suggested transmission of the disease to calves via milk
(Hillerton, 1997), the possibility of such a transmission route should not be
totally ruled out.
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
231
A more recently emerging food pathogen is Enterobacter sakazakii. On
April 12, 2002, FDA alerted health care professionals about this pathogen, which
has been associated with consumption of milk-based infant formulas. E. sakazakii
can cause sepsis, meningitis, or necrotizing enterocolitis in newborn infants,
particularly in premature or immunodeficient infants. Investigations of multiple
outbreaks of E. sakazakii infection occurring in neonatal intensive care units
worldwide over the past several years have associated illnesses with milk-based
powdered infant formulas. To date, FDA is not aware of E. sakazakii infections
among healthy, full-term infants in home settings, nor have illnesses been associ-
ated with liquid infant formulas (FDA, 2002~. The emergence of new or newly
recognized human pathogens that may be transmitted through milk or through
consumption of other animal products highlights the need for food safety regula-
tions that can be changed in a timely and responsive fashion as new hazards are
identified and characterized.
Other Fluid Milk Standards
Although adequate refrigeration, aseptic processing, and a specified sub-
pasteurization heat treatment to separate cream prior to bulk shipment of milk are
processes included in the PMO, only pasteurization and ultrapasteurization
(defined in Table 7.2) are recognized by the PMO as acceptable processes for
removing or deactivating microorganisms in milk (CFSAN, 2002~.
In addition to specific recommendations for pasteurization conditions, chemi-
cal, bacteriological, and temperature standards have been established for grade A
raw milk products intended for pasteurization, as well as for grade A pasteurized
and bulk-shipped, heat-treated milk products (CFSAN, 2002~. For these products,
milk must be cooled to 7°C or less within two hours after milking. Further, the
TABLE 7.2 Minimum Temperature and Times for Fluid Milk Heat
Treatments
High-Temperature, Ultrahigh-
Short-Time Temperature
Country Pasteurization Ultrapasteurization Processing
United Statesa 72°C/15 sec 138°C/2 sec Not definedd
European Economic Communityb 71.7°C/15 sec Not defined 135°C/1 sec
Australia/New ZealandC 72°C/15 sec 132°C/1 sec 132°C/1 sec
a CFSAN (2002).
b EEC (1994).
c ANZFA (2000).
d 21 C.F.R. part 113: "The thermal process and procedures for manufacturing UHT aseptically
processed milk and milk products must comply with U.S. Food and Drug Administration require-
ments for sterilizing low acid foods."
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232
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
blend temperature after the first and subsequent milkings cannot exceed 10°C.
Pasteurized products must not exceed 7°C throughout distribution. Raw milk and
pasteurized products cannot test positive for drug residues as specified in sec-
tion 6 of the PMO (CFSAN, 2002), a chemical performance standard related to
good on-farm practices. Residual phosphatase activity may be measured in
pasteurized products to reflect pasteurization efficacy. Pasteurized products must
have less than 350 munits/L phosphatase activity for fluid products and less than
500 munitslL for other milk products. Table 7.2 provides current standards from
the United States, the European Economic Community (now the European
Union), and Australia and New Zealand for minimum heat treatments for milk
products. Table 7.3 provides microbial and somatic cells limits for raw milk
intended for pasteurized products, and Table 7.4 provides microbial standards for
pasteurized fluid milk products.
Somatic cell count limits for raw milk intended for pasteurized products are
arguably a safety standard, as exceeding these limits may prevent effective appli-
cation of a pasteurizing process. Similarly, the microbial standards for pasteurized
fluid milk products (total bacteria and coliform bacteria) were not implemented
on the basis of food safety per se; instead, the rationale behind these standards is
that keeping total bacteria and coliform cell numbers within the specified limits
reflects good management practices such as equipment cleanliness and sanitation
or refrigeration control, which are essential elements of a food safety program.
TABLE 7.3 Microbial and Somatic Cell Count (SCC) Standards for Raw Milk
Intended for Pasteurized Milk Products
Country
Producer Raw Milka Plant Raw Milkb
United StatesC 100,000 cfu/mLd 300,000 cfu/mL
750,000 SCCe
Canadaf 50,000 cfu/mL 50,000 cfu/mL
500,000 SCC
European Economic Communityg 100,000 cfu/mL 300,000 cfu/mL
400,000 SCC
Australia/New Zealandh 150,000 cfu/mL 150,000 cfu/mL
a Unpasteurized milk before it has left the holding tank on the farm.
b Unpasteurized milk after it has left the farm holding tank.
c CFSAN (2002).
d cfu/mL were measured by aerobic plate count.
e SCC must not exceed 1,000,000 in goat milk.
fCFIS (1997).
g EEC (1994).
h ANZFA (2000).
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
TABLE 7.4 Microbial Standards (per mL) for Pasteurized Milk Products
233
Country Total Bactenaa Coliform Bactenaa
United Statesb 20,000C 10, except in heat-treated, bulk
milk transport tank shipments,
which may not exceed 100
Canadad m = 10,000 m = 1
M= 25,000 M= 10
n=5 n=5
c=2 c=2
European Economic Community After 5 d at 6°C
(EEC)e m = 50,000 m = 0
M = 500,000 M = 5
n=5 n=5
c=1 c=1
Australia/New Zealandf m = 50,000 m = 1
M = 100,000 M = 10
n=5 n=5
c=1 c=1
a Total bacteria (as measured by aerobic plate count) and coliform bacteria counts given as the upper
limit of cfu/mL for the United States. For Canada, EEC, arid Australia/New Zealand, two-tiered
limits are given, with allowable results based on n number of samples, where n = number of sample
units (subsamples) to be examined per lot, m = maximum number of bacteria per g or mL of product
that is of no concern (acceptable level of contamination), M = maximum number of bacteria per g or
mL of product, that if exceeded by any one sample unit (subsamples) renders the lot in violation of
the regulations, c = maximum number of sample units (subsamples) per lot that may have a bacterial
concentration higher than the value for m but less than value for M without violation of the
regulations.
b PHS (1999).
c Not applicable in cultured dairy products.
d CFIS (1997).
e EEC (1994).
f ANZFA (2000).
CHEESE AND OTHER DAIRY FOOD PRODUCTS
As with milk, FDA's Division of Dairy and Egg Safety, Office of Plant and
Dairy Foods and Beverages is also responsible for the development and imple-
mentation of regulations to protect the safety of cheese and other dairy foods that
enter interstate commerce. According to 21 C.F.R. §1240.61, no milk or milk
products in final package form intended for direct human consumption shall enter
interstate commerce unless they are manufactured from pasteurized milk or pas-
teurized milk ingredients, except where alternative procedures are provided for
by regulation, such as in 21 C.F.R. part 133, which contains regulations for
cheeses and related cheese products.
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234
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
Standards of identity have been established for most natural cheeses, process
cheeses, cheese foods, and cheese spreads (21 C.F.R. part 133~. All cheeses
belonging to a given variety must comply with the published standard and must
be labeled with the name prescribed in the standard. In general, identity standards
specify a maximum permissible moisture content and minimum milk fat content.
A few natural cheeses are required to be made from pasteurized milk (e.g.,
Monterey Jack, cream cheese, mozzarella cheese); however, most, including
many soft ripened cheeses (21 C.F.R. § 133.182) and semi-soft cheeses (21 C.F.R.
§133.187), may be made from either raw or pasteurized milk. The regulation
states that "if cheese is labeled as 'heat treated,' 'unpasteurized,' 'raw milk,' or
'for manufacturing,' the milk may be raw or heated at temperatures below pas-
teurization. Cheese made from unpasteurized milk shall be cured for a period of
60 days at a temperature not less than 35°F. If the milk is held more than 2 hours
between time of receipt or heat treatment and setting, it shall be cooled to 45°F or
lower until time of setting" (7 C.F.R. §58.439~. Standards of identity may stipu-
late a holding period longer than 60 days if further aging is required to develop
the characteristics of the cheese variety.
The Scientific Basis for the 60-Day Aging Period for Cheeses
Made with Unpasteurized Milk
Origins
Although not explicitly stated in the regulations, the 60-day holding period
recommendation is intended to provide a measure of pathogen reduction in
cheeses manufactured from milk that has not been pasteurized. This recommen-
dation, which was first published in 1950 (15 C.F.R. §5653), was established by
expert testimony provided during hearings that were conducted during the devel-
opment of the current cheese standards of identity (Personal communication,
J. Mowbray, FDA, September 25, 2002~.
The scientific underpinnings of this recommendation are obscure, but appear
to be derived at least partially from a study that investigated survival of B. abortus
in Cheddar cheese (Gilman et al., 1946~. This study reported that B. abortus
survived for up to 6 months in cheeses that had been artificially inoculated at
levels of approximately 1,000 cfu/mL and held at 4.4°C. Bacterial survival was
monitored directly by culturing viable B. abortus, and indirectly by guinea pig
infection. In these initial experiments, 6-month-old cheeses were reported as
positive for B. abortus, but no numbers were given; guinea pig lesions were
described as slight. When these cheeses had been held for 1 year, inoculated
guinea pigs showed no sign of B. abortus infection (i.e., no blood agglutination
reactions, no characteristic lesions, and no B. abortus recovery from the spleen).
No B. abortus was recovered from commercial Limburger cheeses that had been
held for 57 days (no temperature or other conditions were described), despite the
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
235
fact that the milk used to manufacture two of the cheeses had tested positive for
both viable B. abortus (no numbers given) and for guinea pig infection. Cheddar
cheese made from milk that was naturally contaminated at levels of 700 to 800
cfu/mL was positive for culturable B. abortus (no numbers given) for 3 months.
Viable B. abortus were recovered from some, but not all, of these test cheeses
after 6 months; after 1 year, all guinea pigs were negative for signs of B. abortus
infection. Cheeses made from milk collected from herds positive for B. abortus
(no numbers given for initial levels of B. abortus in cheese milk) were negative
(apparently for the presence of viable B. abortus, but the authors did not distin-
guish between this possibility or whether these negative results reflected guinea
pig inoculation experiments) after storage for at least 41 days at temperatures
ranging from 1.1°C to 2.7°C. Unfortunately, many of the cheeses that were
intended for examination in this part of the study were not tested for the presence
of B. abortus, as samples were lost. Further, initial cheese storage period lengths
were not standardized, but rather ranged from 41 to 84 days, making it very
difficult to compare results among the cheeses. As part of the manuscript discus-
sion, the authors claimed that Cheddar cheese had not been proven as a vector for
human brucellosis (undulant fever), and that typhoid fever epidemics had not
been attributed to cheeses cured for more than 63 days. Therefore, despite their
own laboratory results, they believed that the epidemiological evidence suggest-
ing a lack of association between cheese consumption and disease provided strong
support for an aging period of approximately 2 months for commercial cheeses.
The final stated conclusion was that "an aging period of 60 days is reasonable
assurance against the presence of viable B. abortus organisms in Cheddar cheese"
(Gilman et al., 1946~.
Emerging Food Safety Concerns
Recent evidence of the ability of bacterial pathogens to survive throughout a
60-day holding period has arisen from investigations of outbreaks of foodborne
illnesses that have been traced back to aged cheeses, as well as from additional
scientific research. Specifically, three outbreaks of salmonellosis following con-
sumption of Cheddar cheese, two in Canada and one in the United States, suggest
that various Salmonella strains can survive for extended periods in cheese prod-
ucts, as described below.
In the first outbreak, which was traced to Cheddar cheese manufactured in
Kansas in 1976, raw milk had been held without refrigeration in the processing
plant for 1 to 3 days prior to pasteurization and cheese manufacture. While it is
not known for certain, total bacterial numbers in the prepasteurized, raw milk
could have exceeded the thermal destruction capacity of the pasteurizing process.
Microbiological analyses revealed the presence of Salmonella Heidelberg at very
low levels (0.36-1.8 cfu/100 g of cheese) in the aged cheeses. The average pH of
cheese batches bearing Salmonella was 5.6 vs. 5.4 for uncontaminated product;
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
Food Safety Policy for Imported Cheeses
237
FDA is charged with enforcing the Federal Food, Drug and Cosmetic Act,
along with other laws that are designed to protect the health of consumers. These
laws apply equally to domestic and imported products. Therefore, as with domes-
tic products, imported foods must be pure, wholesome, safe to eat, and produced
under sanitary conditions. All products must contain truthful and informative
labeling in English. Under some circumstances, based on past history of a product
or on other information indicating that a product may be violative, imported
products may be detained upon arrival into the United States. FDA can identify
and detain products from an entire country or geographic region if violative
conditions appear to be widespread (this procedure is called "detention without
physical examinational. Cheeses and other dairy foods have occasionally been
subjected to detention. For example, due to widespread contamination with
L. monocytogenes, French cheese was ordered to be detained in mid-1986. This
action occurred despite a French program that already had been implemented in
1974, which allowed only plants that were certified by the French government to
be following good manufacturing practices to export soft-ripened cheese to the
United States. In January 1987, this certification program was expanded to include
a requirement for the use of pasteurized milk in the manufacture of soft-ripened
cheeses, as well as for Listeria testing of those products intended for export to the
United States. Currently, only French processing plants that are certified by the
French Ministry of Agriculture to export soft-ripened cheese manufactured from
pasteurized milk can legally market their products in the United States. The
FDA's Office of Regulatory Affairs maintains a listing of products that are cur-
rently subject to import action.
The Food and Drug Administration Food Compliance Program for
Domestic and Imported Cheese and Cheese Products
In response to a stated increase in the association of cheese and cheese
products with outbreaks of human illness, in 1998 FDA issued a Food Compliance
Program document that detailed plans for inspecting domestic cheese firms;
examining domestic and imported cheeses for microbiological contamination,
phosphatase, and filth; and taking action on cheese lots when violations are
detected (CFSAN, 1998~. Sampling priorities were established in the following
order: soft cheeses, hard cheeses, and cheese products. When cheese samples
are taken as part of this program, mandated analyses include testing for
L. monocytogenes, Salmonella, E. colt, enterotoxigenic E. cold (enterotoxigenic
E. cold analyses are performed only when E. cold are present at levels of 104/g),
E. cold 0157:H7, Staphylococcus aureus, and phosphatase. The testing is per-
formed as a result of a public health concern and with the objective of identifying
contaminated product and keeping it off the market; therefore, the sampling is not
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SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
designed for batch-to-batch or process verification purposes. Samples are col-
lected during scheduled inspections when either of the following criteria are met:
(1) the firm's products have a previous history of microbiological contamination
(e.g., as a follow-up to a complaint or illness), or (2) sampling is conducted for
some specific reason (e.g., observations during inspection indicate that sampling
is warranted). This program is an example of a finished-product testing strategy
initiated in response to illnesses associated with specific foods.
THE ROLE OF THE U.S. DEPARTMENT OF AGRICULTURE IN
DAIRY PRODUCT QUALITY AND WHOLESOMENESS
Dairy Products Grading and Inspection Program
In addition to FDA oversight of dairy product safety, many U.S. dairy plants
participate in a voluntary grading and inspection program offered by the U.S.
Department of Agriculture (USDA) through its Agricultural Marketing Service
(AMS). USDA inspection and grading services are performed under the regula-
tions in 7 C.F.R. part 58. The overarching goal of the AMS inspection and
grading program is "to aid in the marketing of milk and dairy products by provid-
ing a common language of trade through the development, improvement, and
interpretation of standards, specifications, and quality improvement programs"
(AMS, 2002~. The specific objectives of the program are to develop, maintain,
and disseminate (1) sanitary requirements and model regulations to enhance the
availability of safe, wholesome, high-quality dairy products, (2) definitions for
product quality and wholesomeness, (3) requirements for participation in the
USDA-Approved Dairy Plant Program, and (4) model state requirements for
sanitary production and processing of manufacturing grade milk and milk products.
The USDA grading program was initiated in the early 1900s as a conse-
quence of a recognized need for a common language for dairy product character-
istics. The Office of Markets, which predates the AMS, was established in 1913
to lay the groundwork for dairy market news and product standardization and
grading. The Dairy Grading Branch of AMS currently administers this program.
Plants participating in this program are inspected at least twice yearly. Plant
inspections are unannounced and cover more than 100 items, including milk
supply, plant facilities, equipment condition, sanitary practices, and processing
procedures. AMS publishes specifications to guide dairy plants toward meeting
approval requirements (Dairy Division, 2002~. In some cases, buyers may require
that products meet specifications or grade standards. Therefore, despite a fee
required to participate, this voluntary program is widely used by the dairy indus-
try (AMS, 2002) because it provides guidance regarding how to achieve these
quality standards.
Although almost all dairy products can be inspected or graded, the products
most commonly inspected and graded are butter, Cheddar cheese, and instant and
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
239
regular nonfat dry milk (AMS, 2002~. Official USDA grades (e.g., U.S. Grade
AA for butter and Cheddar cheese and U.S. Extra Grade for nonfat dry milk) are
derived from uniform standards of quality developed by the Standardization
Branch of USDA. An official USDA grade indicates the product's quality by use
of designated letters such as "AA" or words such as "extra" (AMS,2002~. Product
specifications reflect minimum acceptable requirements for dairy products for
which official grade standards have not been determined. The official USDA
quality approved shield can be applied to products that meet the requirements of
a specification. USDA standards and specifications are designed to ensure that
products are free from defects that affect usability, which include, but are not
limited to, the state of preservation of the product, cleanliness, wholesomeness,
and fitness for human food (7 C.F.R. part 58~.
Development of USDA product standards and specifications is usually initi-
ated by requests from outside USDA, often as a consequence of the development
of a new product or a change in processing technology (AMS, 2002~. Many
requests are industry-driven, but other groups may initiate the process as well.
Standard and specification development includes four elements: (1) research to
determine quality factors and the range of quality encountered for the product,
(2) investigation of production practices, including types of processing operations,
packing, and equipment used, and consumer buying practices, (3) a statistical
plan for product sampling, and (4) interviews with producers, packers, processors,
shippers, receivers, consumers, and scientists. The standards and specifications
are field-tested after the research is completed. At the end of this process, the
standard or specification is published in the Federal Register. Standards and
specifications increasingly rely upon scientific measurements, microscopic exami-
nations, and written descriptions of quality aspects, but the process is still largely
subjective (AMS, 2002~. Conformance to standards and grades is largely based
on the grader' s perception of product taste, smell, appearance, and feel. Standards
and specifications are reviewed and updated periodically to reflect changes in
technology and milk quality (AMS, 2002~.
Milk for Manufacturing Purposes
Milk for manufacturing purposes includes "milk produced for processing
and manufacturing into products for human consumption but not subject to
Grade A or comparable requirements" (AMS, 2002~. USDA has established
bacterial standards for milk to be used for manufacturing purposes. The goal of
these requirements is to promote uniformity in state dairy regulations and laws,
which should promote national uniformity in the sanitary processing of milk for
manufacturing purposes. Enforcement of manufacturing milk regulations lies
solely with the states. Lists of recommended microbiological standards for raw
milk intended for manufacturing purposes and of AMS dairy product grade
standards are presented in the tables in Appendixes F and G.
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SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
THE USE OF CURRENT STANDARDS AND CRITERIA
UNDER HACCP
As described earlier, through evolution of the PMO and other dairy stan-
dards, the dairy industry has a long history of application of regulations to ensure
the safety of its products intended for interstate commerce. Nevertheless, NCIMS
has proposed testing the Hazard Analysis and Critical Control Point (HACCP)
system under NCIMS as an alternative to the traditional dairy inspection/rating/
check system. In 1997, NCIMS conference delegates voted to evaluate the possi-
bility of implementing HACCP systems in the dairy industry, and in 1999 they
voted to implement a voluntary HACCP pilot program. The NCIMS HACCP
committee has had oversight responsibilities for implementation of this pilot
program since 1999. One of the greatest challenges facing the dairy industry has
been the incorporation of HACCP into the regulatory format already in place.
The NCIMS proposal has been developed in ways that harmonize HACCP with
traditional NCIMS requirements, in terms of regulatory reciprocity and over-
sight. For example, NCIMS proposes that the role of FDA in dairy HACCP could
be similar to its current oversight and technical assistance role in the NCIMS
system. The current regulatory authority is envisioned to perform the HACCP
auditing function to verify that HACCP plans are effective.
Implementation of HACCP requires establishing prerequisite programs such
as Good Manufacturing Practices and Standard Sanitary Operating Procedures.
Various aspects of these programs (e.g., safety of process water, condition and
cleanliness of food contact surfaces, prevention of cross-contamination, control
of employee health conditions and personal hygiene facilities, proper labeling
and storage of toxic compounds, and pest exclusion) are already addressed in
various sections of the existing PMO. Hence, the dairy industry already has in
place the background Good Manufacturing Practices and Standard Sanitary
Operating Procedures to reduce the potential occurrence of food safety hazards.
The most likely critical control points for dairy processing operations will be
pasteurization time and temperature conditions and control of raw and processed
product storage temperatures. Microbial specifications and standards have been
and will continue to be used for regulatory purposes in the dairy industry; how-
ever, microbiological CCPs are unlikely to be adopted in the dairy industry.
In July 1999, applications to participate in the dairy HACCP pilot program
were sent to all 50 states by the NCIMS HACCP committee. Of 16 dairy industry
applicants, 6 plants representing 6 states were chosen to participate. To provide
essential ongoing technical support for the participating plants and state regula-
tors, NCIMS and FDA's State Training Branch have held HACCP training work-
shops for program participants. Further, the NCIMS HACCP established a Tech-
nical Resource Team comprised of FDA, state, and industry representatives.
Questions are generally submitted by e-mail, and responses are posted on the
NCIMS HACCP website (CFSAN, 2003~. In May 2001, the NCIMS Conference
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
241
extended the pilot program to 2003 and expanded the program to invite all
Grade A plants to participate. The pilot program now includes 15 plants in
10 states. The dairy processing industry's continued participation in this program
will help to promote the continued availability of the NCIMS HACCP program
as a voluntary alternative to the more prescriptive PMO program.
The committee commends the dairy industry for voluntarily implementing a
HACCP pilot program and strongly encourages timely adoption of HACCP
systems throughout various sectors of the dairy processing industry. Adoption of
performance standards for pathogen reduction, such as that proposed for cheese
manufacturing, would more appropriately fit into a HACCP framework than in
the dairy industry's current regulatory system.
ARE THE STANDARDS AND SCIENTIFIC CRITERIA FOR MILK
AND DAIRY PRODUCTS ACHIEVING THEIR GOAL?
The committee recognizes that the application of regulations within the
evolving PMO has been directly credited with reducing the incidence of milk-
borne disease (Olsen et al., 2000~. To illustrate this point, the 1999 revision of the
PMO stated that 25 percent of all disease outbreaks due to contaminated food and
water were a consequence of consumption of milk products in 1938, but that,
more recently, the prevalence of milk-borne disease has dropped to less than
1 percent of reported outbreaks.
While dairy foods appear to be responsible for a relatively small proportion
of U.S. foodborne-illness outbreaks that currently are successfully tracked to
their source, occasional outbreaks of illness from consumption of contaminated
dairy products do occur. The outbreaks listed in Table 7.5 do not provide a
comprehensive listing of dairy food-associated illnesses since 1985, but rather
provide a description of a selection of outbreaks associated with an international
variety of dairy products, a variety of foodborne pathogens, and a variety of
routes of product contamination. The goal of the table is to illustrate routes of
entry for foodborne pathogens in dairy products. Determination of patterns among
outbreak incidents may assist in identifying the most effective interventions and
allocation of resources to further reduce dairy food-associated illnesses.
Of the 20 outbreaks listed in Table 7.5, 11 are associated with consumption
of raw milk products or of products contaminated by raw milk or by close contact
with farm animals. These outbreaks further illustrate the possibility of the pres-
ence of microbiological hazards in unpasteurized milk, as well as the need to
develop effective interventions to control pathogens on the farm. Nine outbreaks
(including some of those associated with raw milk product consumption) were
associated with postpasteurization contamination of processed products. Post-
pasteurization contamination usually results from lapses in cleaning and sanitizing
procedures or from human food handling or processing errors that compromise
product safety. The outbreak in 1988 brings into question the adequacy of current
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242
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
TABLE 7.5 Outbreaks of Foodborne Disease Associated with Dairy Products
Year Product and/or Source
Organism
1985 Mexican-style soft cheese, illegally imported, raw milk suspected
1985 Mexican-style white cheese, environment and equipment grossly contaminated,
even after clean-up; raw-milk delivery allegedly exceeded pasteurization capacity
1985 Pasteurized 2% milk; postpasteurization contamination; pipe cross-connection
appears to have allowed raw milk to commingle with pasteurized
Brucella
Listeria ~
Salmonell
1988 Pasteurized milk; spores of Bacillus survived pasteurization and grew during B. cereus
subsequent storage at refrigeration temperatures
1989 Mozzarella manufactured at a single plant, or cross-contaminated by a batch from S. Javiana
that plant; low-level contamination of nationally distributed food product caused S. Oranier
geographically dispersed foodborne outbreak that was difficult to detect
1992 Imported Irish soft unpasteurized cows' milk cheese (import into UK temporarily S. Dublin
stopped, resumed after manufacturer decided to pasteurize milk used in production
of cheese for export)
1994 Chocolate milk, leaking equipment, L. monocytogenes in plant environment, poor L. monoc
sanitation, postpasteurization contamination, insufficient cooling
1994
1994
2000
Unpasteurized soft cheese cross-contaminated by chicken carcass (chickens
dressed by cheese makers)
Ice cream, contaminated through transport of pasteurized ice cream premix in
tanker trailers that had previously carried nonpasteurized liquid eggs containing
S. Enteritidis
1996 Formula dried milk for infants, international outbreak
1997 Raw milk, contaminated by cows at dairy of origin
1997 Mexican-style soft cheese made with raw milk
1998 Fresh cheese curds, unpasteurized, mislabeled as pasteurized
2000 Bottled pasteurized milk, possibly postpasteurization contamination from pigs
via rinsing with untreated well water
Fluid milk products; milk products formulated with skim milk powder bearing
staphylococcal enterotoxin A
2000
2001
2002
S. Berta
S. Enteriti
Morbier cheese, one batch from a single processing plant incriminated
(unpasteurized)
Mexican-style soft cheese
Raw milk obtained through cow-lease program, strategy used to circumvent
legislation that prohibits sale of unpasteurized milk in this state
2002 Visit to dairy farm with E. coli-infected cows and calves
2003 Farmstead Gouda cheese; source under investigation
S. Anatun
E. cold O]
S. Typhin
E. cold O]
Yersinia e
Staphyloc
enteroto'
producec
S. Typhin
L. monoc'
Campylob
E. cold O
E. cold O
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
'roducts
243
Organism
Number of Cases Location Reference
Brucella melitensis 9 TX Altekruse et al., 1998
nated, Listeria monocytogenes 145 CA Boor, 1997
n capacity
Cation Salmonella Typhimurium 16,000 culture IL Ryan et al., 1987
confirmed;
168,791 to
197,581 cases
estimated
ring B. cereus 280 The Netherlands Van Netten et al., 1990
tch from S. Javiana, 164 WI, MN, MI, NY Hedberg et al., 1992
ct caused S. Oranienberg
t
rporarily S. Dublin 42 UK (South-east Maguire et al., 1992
production England)
nt, poor L. monocytogenes 45 IL Dalton et al., 1997
ns S. Berta 82 Ontario Ellis et al., 1998
ix in S. Enteritidis 224,000 MN Hennessy et al., 1996
containing (estimate)
S. Anatum 19 France, UK Threlfall et al., 1998
E. cold 0157:H7 6 OR Keene et al., 1997
S. Typhimurium DT104 54 WA Villar et al., 1999
E. cold 0157:H7 55 WI Durch et al., 2000
pigs Yersinia enterocolitica 10 VT, NH Ackers et al., 2000
aring
Staphylococcal
enterotoxin A,
produced by S. aureus
S. Typhimurium
14,700 Japan
113
Asao et al., 2002
De Valk et al., 2000
L. monocytogenes 3 NC Boggs et al., 2001
nt Campylobacter jejuni 5 WI CDC, 2002
E. cold 0157:H7 51 PA Crump et al., 2002
E. cold 0157:H7 11 Alberta CFIA, 2003
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244
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
pasteurization practices for destruction of spore-forming organisms (e.g., Bacillus
cereus) that can reproduce in fluid milk, particularly in those products that may
be stored at refrigeration temperatures for extended times. In general, the presence
of spore-forming organisms in raw milk that might not be destroyed by pasteuriza-
tion has not been considered a significant public health risk (CFSAN, 2002~.
Additional research, targeted at exploring the survival and outgrowth of spore-
forming pathogens in conventionally pasteurized milk that is at refrigeration
temperatures for more than 7 days, may be warranted. Finally, one large-scale
outbreak in 2000 resulted from poor manufacturing practices in combination with
reprocessing of past-code-date fluid milk products. Out-of-date cartons of fluid
milk that had been delivered to a powdered milk processing plant were reportedly
opened by hand and poured into vats that were not properly refrigerated. A
subsequent power outage prevented the milk from being pasteurized for many
hours. As a consequence, the milk was held for an extended period at tempera-
tures permissive for bacterial growth. S. aureus was probably introduced into the
milk during handling. This organism is predicted to have multiplied to levels
necessary for enterotoxin production (> 100,000/mL) in the warm milk. After the
electricity was restored, the milk was pasteurized, but conventional pasteuriza-
tion conditions do not inactivate staphylococcal enterotoxin A. The milk was
then dried into powdered milk ingredients. The resulting powdered milk ingredi-
ents were used to formulate fluid milk products, which also were pasteurized.
The presence and persistence of the enterotoxin from the powdered milk ingredi-
ents in the pasteurized fluid milk products illustrates the toxin' s ability to with-
stand conventional heat processing treatments and highlights the importance of
preventing bacterial contamination of, and maintaining temperature control over,
perishable food products.
The committee concludes that the reduction in foodborne illnesses associ-
ated with milk consumption in the United States is primarily a consequence of the
near universal implementation of milk pasteurization for commercial fluid milk
products, and also reflects the implementation of sanitation programs in process-
ing plants that are designed to protect pasteurized milk from recontamination
with pathogenic microbes. The committee further recognizes that despite the
clear link that has been established between raw milk consumption and foodborne
illnesses, some consumers continue to drink raw milk. The committee recom-
mends that state and local authorities ban the sale of unpasteurized milk because
of its inherent risks. Because most unpasteurized milk is sold or consumed at the
farm, targeted educational programs that illustrate the hazards of raw milk con-
sumption are warranted. FDA and state authorities should consider requiring
clear and concise labeling to identify cheeses manufactured from unpasteurized
milk to assist members of the public in making informed choices regarding food
purchase and consumption.
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CONTROLS FOR HAZARDS IN DAIRY PRODUCTS
ECONOMIC AND ADMINISTRATIVE FEASIBILITY OF MILK
PASTEURIZATION
245
Virtually all fluid milk processors that ship milk products via interstate
commerce have invested in equipment for pasteurizing their product. Manufac-
turers of cheese from milk that has not been pasteurized must hold the product for
a minimum of 60 days at a temperature not less than 35°F. The expense of
holding this inventory for the required time is part of the input cost of cheese
manufactunng. As a measure for controlling numbers of bacterial pathogens,
pasteurization of fluid milk and other products and holding times for cheeses are
economically feasible and commonly applied.
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Representative terms from entire chapter:
milk products
