PART D: SCIENCE BASE
Section 9: Food Safety
This section addresses two major questions related to food safety, which
led to two conclusive statements:
- What behaviors are most likely to prevent food safety problems? Or,
in terms of how food is handled, what behavior(s) are most likely to cause
food safety problems (foodborne illness)?
Subsumed under this question were more specific questions, such as "What
data are there regarding the effectiveness of bacterial cleansers in preventing
foodborne illness?" and "What are the data regarding cleaning fruits and
vegetables to reduce the risk of foodborne illness?"
The general search strategy used to find the scientific evidence related
to this broad question appears in Part C, Methodology. See the summary
table in Appendix G 3 for a table summarizing the findings from a search
on hand washing.
As a part of its search, the Committee also collected data related to
an educational tool for conveying messages to consumers about safe food
handling and preparation. In particular, the Committee obtained information
on a national public education campaign called FightBAC! and addressed
the following question:
- What topics, if any, need attention even though they are not an integral
part of the "FightBAC!®" campaign? (FightBAC! is a national public
education campaign to promote food safety to consumers and educate them
on how to handle and prepare food safely. In this campaign, pathogens
are represented by a cartoon-like bacteria character named "BAC.")
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SCOPE OF THE PROBLEM
Foodborne diseases cause approximately 76 million illnesses, 325,000 hospitalizations,
and 5,000 deaths in the United States each year (Mead et al., 1999). Known
pathogens account for an estimated 14 million illnesses, 60,000 hospitalizations,
and 1,800 deaths. Three pathogens—Salmonella, Listeria,
and Toxoplasma—are responsible for more than 75 percent of these
deaths. Unknown agents account for the remaining 62 million illnesses, 265,000
hospitalizations, and 3,200 deaths. The actual percentage of outbreaks of
foodborne illness is likely to be much larger than described above because
small outbreaks that occur in homes often are unreported or not investigated
Although most foodborne infections cause mild illness,
severe infections and serious complications—including death—do occur. As
described by the FoodNet Working Group (Angulo et al., 1998), the public
health challenges of foodborne diseases are changing rapidly as a result
of newly identified pathogens and vehicles of transmission, changes in food
production, and an apparent decline in food safety awareness. Americans
are exposed to foodborne pathogens from distant parts of the United States
and the world. Increased demand for ready-to-eat and minimally processed
foods and increased consumption of food in eating establishments outside
of the home also have contributed to new exposures to foodborne disease.
For example, foodborne disease outbreaks of Salmonella and Escherichia
coli O157:H7 infections have been associated with an increasingly wide
variety of foods, including some previously thought to be safe, such as
alfalfa sprouts and unpasteurized fruit juice.
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QUESTION 1: WHAT BEHAVIORS ARE MOST LIKELY TO PREVENT FOOD SAFETY
The behaviors in the home that are most likely to prevent a problem with
foodborne illnesses are
Cleaning hands, contact surfaces, and fruits and vegetables (but not
meat and poultry, which should not be washed)
Separating raw, cooked and ready-to-eat foods while shopping, preparing,
Cooking foods to a safe temperature
Chilling (refrigerate) perishable foods promptly
The Four Basic "FightBAC!" Educational Messages
The four main messages of the food safety guideline emphasize proper food-handling
behaviors (clean, separate, cook, chill) and coincide with the FightBAC!
campaign of The Partnership for Food Safety Education, created in 1997 by
the U.S. Departments of Agriculture, Education, and Health and Human Services,
and 10 food industry organizations (www.fightbac.org).
The FightBAC! messages were developed from a consensus of food safety experts
and have been tested for consumer comprehension. Large improvements in consumer
food safety practices have been seen since the campaign has been in effect,
and a recent survey found that these gains have been maintained or improved
for all four food-handling practices (FDA, 2002). A survey of 500 Latino
consumers (Dharod et al., 2004) showed that the influence of the FightBAC!
campaign is likely to improve food safety awareness and bring about changes
in food safety knowledge and attitudes.
Affirmation of the usefulness of the FightBAC! messages was demonstrated
by Bryan (1988) who surveyed all the pertinent literature of the time on
factors that contribute to outbreaks of foodborne disease. His sources included
food surveillance data on foodborne illness submitted to the Centers for
Disease Control and Prevention (CDC), surveillance data from health agencies,
investigations made by CDC personnel, and articles published in public health,
medical, or food science journals. He ranked the order of practices likely
to contribute to foodborne illness as follows
In a viewpoint paper based on data from CDC, Medeiros et al. (2001a) developed
food safety consumer education messages as follows
- Primary messages
- Hand washing
- Adequate cooking
- Avoiding cross-contamination
- Secondary messages
- Keeping food safe to eat
- Avoiding food from unsafe sources
Using a four-round Delphi technique, Hillers et al. (2003) identified and
ranked food-handling and consumption behaviors associated with 13 major
foodborne pathogens. They surveyed 40 nationally ranked experts: 11 in food
microbiology, 9 in epidemiology, 10 in food safety education, and 10 in
food safety policy. Hiller and colleagues concluded that the acts of primary
importance in the prevention of foodborne illness were
Using a thermometer to cook foods adequately
Avoiding certain foods likely to be contaminated
The identification and ranking of the causes of food safety problems and
corrective measures above is limited by shortcomings in the source data
that result from incomplete and inadequate reporting of outbreaks and incomplete
write-up or abstracting of contributing factors. Moreover, in the Hillers
et al. (2003) study, some bias could have resulted from the use of expert
opinions, processing of the opinions by a research team, and a requirement
that respondents respond in fixed ways. Nonetheless, these findings are
based on input from geographically dispersed experts and could lead to a
clearer understanding of key concepts needed to educate consumers for safer
food handling and reducing risks of foodborne illness.
Further affirmation of the FightBAC! messages was presented by Sulka et
al. (2003). Contributing factors for E. Coli 0157:H7 and Salmonella
enteritidis outbreaks are listed as inadequate/improper cooking, contamination,
pre-harvest contamination, ill food handler, and improper storage or holding
The Committee found evidence to support additional food safety guidance,
as summarized below.
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The "Clean" Message
Hand Washing. The Committee identified five
useful papers that addressed hand washing. The strongest paper was the double-blind,
placebo-controlled study by White et al. (2001), which included structured
hand hygiene education. The study assessed whether an alcohol-free hand
sanitizer containing the surfactants allantoin and benzalkonium chloride
could reduce illness and absenteeism among elementary school children and
serve as an effective alternative when regular soap and water hand washing
was not readily available. Although the study did not compare the sanitizer
to soap and water, the importance of hand washing was evident from the results:
after 5 weeks, students using the active product were 35 percent less likely
to have been absent because of illness when compared with the placebo group.
Although the study lacked a cross-over confirmation and it lost a large
portion (55 percent) of the original study participants because of a lack
of compliance in many of the study classrooms, this study demonstrated that
there are simple ways to overcome obstacles of adequate hand washing, including
education. The results demonstrate that there is opportunity for proper
hand washing at the school level and, consequently, for improving attendance
and promoting the health of students.
Charbanneau and colleagues (2000) provided direct data demonstrating the
value of washing hands with a mild soap. They found that 20-second soap-and-water
hand washing was more effective than using hand sanitizers containing 70
percent ethanol in eliminating viable bacteria from meat-soiled hands. The
Food and Drug Administration (FDA) and the CDC (2004) recommend soap and
water cleansing for food handling, noting that alcohols have very poor activity
against bacterial spores, protozoan oocyts, and certain nonenveloped viruses.
Further evidence supporting soap-and-water hand washing is provided by
a study conducted by Master et al. (1997). When compared with usual hand
washing practices, washing the hands a minimum of four scheduled times a
day in addition to usual hand washing produced a statistically significant
(p=0.0024) decrease in the number of absences due to gastrointestinal illness
(18.5 days of absence in the hand washing group versus 49 days of absences
in the control group). Reported overall illness-related absence was lower
but not significantly different. The major limitations of the study include
the use of a single institution, the use of a discrete population without
socioeconomically diverse backgrounds and lack of double-blindedness.
A study in an adult day care center (Falsey et al., 1999) and another
of telephone interviewees (Mead et al., 1997) provide indirect evidence
supporting the value of hand washing in the prevention of infections. Although
these two studies have some limitations, the authors provide a sound basis
for their estimates that thorough hand washing reduces infections by about
one-half and one-third, respectively.
These five studies support the inclusion of the detailed hand washing
protocol developed by the CDC (http://www.cdc.gov/ncidod/op/handwashing.htm) in food safety guidance. In addition, to reduce the risk
of cross-contamination, add to the protocol guidance regarding drying hands
using a clean disposable or cloth towel.
Box 1. Food Safety
Hand Washing Protocol
First, wet your hands and apply liquid or clean
bar soap. Place the bar of soap on a rack to drain.
Next, rub your hands vigorously together and scrub all surfaces.
Continue for 10 to 15 seconds or about the length
of a little tune. It is the soap combined with
the scrubbing action that helps
dislodge and remove germs.
Rinse hands well, and dry them using a clean disposable or cloth
(Adapted from Centers for Disease Control and Prevention, An ounce
of prevention: keeps the germs away.)
Washing Fresh Fruits and
a systematic search of the literature, the Committee identified
10 relevant articles on washing fruits and vegetables,
and experts directed them to
additional useful scientific literature (See Summary Table
in Appendix G-3). Recent outbreaks of foodborne illness
associated with eating fresh produce
have heightened concerns that these foods may be an increasing
source of illness (Tauxe et al., 1997). Studies have
shown that bacteria can survive
and/or grow on fresh produce and that fresh produce supports
the growth of pathogens such as E coli 0157:H7,
Salmonella Montevideo, and Shigella
flexneri (Li-Cohen and Bruhn, 2002; Li-Cohen et al.,
2002). Moreover, some consumers practice unsafe handling
of fresh produce (Li-Cohen and Bruhn,
Consumer surveys demonstrate a growing public concern about food safety
and the need for an explanation behind food safety guidance (Li-Cohen et
al., 2002). Therefore, consumers should be given clear directions on how
to remove pathogens from raw fruits and vegetables. Although washing is
only partially effective at removing pathogens from fresh produce, washing
is the only method that consumers have to reduce pathogen load on fresh
produce (Medeiros et al., 2001b). Food safety information should be simple
to read and easy to follow, such as that developed by Li-Cohen et al. (2002).
Consumers may be unwilling to adopt safe practices if instructions are too
time-consuming or are viewed as costly or inappropriate (Li-Cohen et al.,
Box 2. Food Safety
Protocol for Washing Fresh Fruits and Vegetables
Remove and discard the outer leaves from vegetables such as lettuce
and cabbage before washing
Wash fruits and vegetables (including organically grown, farmer's
market, and homegrown produce) just before cooking or eating
Wash under running potable water
When possible, scrub fruits and vegetables with a clean scrub
brush or with hands
Dry fruits and vegetables
(Adapted from Li-Cohen et al., 2002)
Free moisture on produce may promote survival and growth of microbial populations
in an otherwise inhospitable environment (FDA, 2001). Therefore, Step 5
above is critical if the food will not be eaten or cooked right away. Additionally,
consumers should read the labels of bagged produce to determine if it is
ready-to-eat. Ready-to-eat, prewashed bagged produce can be used without
further washing if kept refrigerated and used by the "used-by" date. If
desired, prewashed, ready-to-eat produce can be washed again (FDA, 2001).
Guidance for Safely Using Bagged Produce.
Read the labels of bagged produce to determine if it is ready-to-eat
Ready-to-eat, prewashed bagged produce can be used without
further washing if kept refrigerated and used by the
If desired, prewashed, ready-to-eat produce can be washed again
Use-by dates should be differentiated from purchase-by dates. Products
with purchase-by dates can be used after that date; however, products with
use-by dates should not be used after the use-by date.
Although some studies have shown that antibacterial agents are proven effective
in reducing indigenous flora on produce such as lettuce during food service
preparation (Smith et al., 2003), these solutions warrant additional testing
and research in household settings.
Washing Meat and Poultry. Washing
raw poultry and meat creates the danger of cross-contamination
and is not necessary
because bacteria on the surface of the meat will be destroyed
by cooking. Washing these foods can allow bacteria that
is present on the surface of
the meat or poultry to spread to other ready-to-eat foods
(FSIS, 1999). Washing raw meat and poultry is reported to
be one of the most commonly
observed food preparation practices that can lead to cross-contamination
(presentation to the Partnership for Food Safety Education
Partners, Inc., June 5, 1997). Literature is not available
on the effects of washing fish, but it would seem that the
same risk for cross-contamination
Cleaning Refrigerators. Cleaning is closely linked
with the problem of cross-contamination—the transfer of harmful bacteria
to food from other foods, often through an intermediary. Refrigerator surfaces
can become contaminated from contact with high-risk foods such as raw meats,
poultry, fish, uncooked hotdogs, certain deli meats, or raw vegetables.
If not cleaned, affected refrigerator surfaces can, in turn, serve as a
vehicle for contaminating other foods.
Even at recommended refrigerator temperatures of 40° F.
or lower, foods such as meat, poultry, fish, and cheese
made from unpasteurized milk have
in common the ability to support the growth of the bacterium Listeria
monocytogenes during extended refrigerated storage
(HHS/USDA, 2003). Ingesting food contaminated with this
organism can be the source of very
serious foodborne illness in high-risk populations. (See
Table E 26.) In a refrigerator that is not kept clean, for
if the liquid from uncooked
hotdogs contains Listeria monocytogenes and it contaminates
refrigerator surfaces, foods coming in contact with those
surfaces may become unsafe
to eat (Byers et al., 1994).
Although other pathogenic organisms grow very slowly at recommended refrigerator
temperatures, cross-contamination that occurs in the refrigerator can lead
to foodborne illness, especially if combined with other unsafe food practices
such as allowing the food to stand at room temperature before eating or
heating the food inadequately. An emphasis on cleaning refrigerators is
consistent with the contribution that cross-contamination makes to foodborne
illness, as reported by Sulka et al. (2003).
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Minimizing the Refrigerator as a Source of Cross-Contamination.
The refrigerator should be cleaned regularly, including the washing
of shelf surfaces and drawers
Liquids should not be allowed to drip or spill from higher refrigerator
shelves onto lower shelves; wipe up spills immediately – clean surfaces
thoroughly with hot, soapy water; then rinse
Liquids from foods such as hot dogs and luncheon meats should not be
allowed to come in contact with other foods or surfaces after the package
is opened (USDA, 2004)
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The "Separate" Message
Bacterial contamination in raw meat and poultry juices, produce, perishable
ready-to-eat foods, and cooked foods can be spread to other foods, utensils,
and surfaces. Its relationship with the "clean" message is discussed briefly
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The "Chill" Message
Based on discussion with food safety experts and Bryan's analysis (Bryan,
1988), the Committee recognized the value of including more than one "chill"
step in the FightBac! sequence (e.g., clean, separate, chill, cook, chill).
Chilling provides substantial protection at any stage of food handling during
which raw foods are not being cleaned or cooked.
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The "Cook" Message
Consumers make many food-handling errors during food preparation
that increase their risk of foodborne illness. Furthermore,
very few consumers
use a food thermometer and they frequently undercook meat
and poultry (Anderson et al., 2004). The best way to tell
if meat, poultry, or egg dishes are
cooked to a safe temperature is to use a thermometer.
The U.S. Department of Agriculture (USDA) and the Food and
Drug Administration (FDA) summarize the following recommendations
for cooking safely:
A thermometer is used to measure the internal temperature of cooked
meat and poultry and egg dishes to make sure that the meat or dish is
cooked all the way through. Minimum safe internal temperatures are as
If using a microwave oven, care is needed to be sure that all parts of
the food reach the specified temperature.
Information from the CDC links eating undercooked, pink ground beef with
a higher risk of illness. If a thermometer is not available, it is advisable
not to eat ground beef that is still pink inside. Cook fish until it is
opaque and flakes easily with a fork.
In 1996 to 1997, FoodNet, a collaborative program among the CDC, USDA,
FDA, and selected State health departments, conducted a telephone survey
of 7,493 adults in 5 states (California, Connecticut, Georgia, Minnesota,
Oregon) to determine the prevalence of risk factors of foodborne illness.
Results indicated that undercooked eggs (runny eggs) were the most commonly
consumed high-risk food, eaten by 19 percent of the respondents in the 5
days before the interview. The researchers concluded that health education
should emphasize the importance of cooking eggs well in order to prevent
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QUESTION 2: WHAT TOPICS, IF ANY, NEED ATTENTION EVEN THOUGH THEY
ARE NOT AN INTEGRAL PART OF THE "FIGHTBAC!" CAMPAIGN?
Avoiding higher-risk foods is an important protective measure (e.g., deli
meats and frankfurters that have not been reheated to a safe temperature
may contain Listeria). This is especially important for high-risk
groups (the very young, pregnant women, elderly and those who are immunocompromised).
Potentially unsafe foods fall in three categories: those having been stored
in a manner or for a period of time that would allow dangerous growth of
bacteria, foods at high risk for contamination by Listeria, and
fish exposed to methylmercury.
Improperly Stored Foods
Not all bacterial growth causes a food's surface to discolor or smell
bad. For example, Larson and Johnson (1999) reported that botulinal toxin
formation occured before overt spoilage occurred in cubed, packaged melons.
Similarly, Lubin and colleagues (1985) found that hard-cooked eggs that
contained toxins did not always produce unacceptable odors or a change in
appearance that was detected. When there is any doubt about the safety of
fresh or leftover foods, for example, when refrigerated leftovers have been
stored for 3 to 4 days, it is advisable to discard them safely, not to taste
Listeriosis, Those at High Risk, and High-Risk Foods
A recent quantitative risk assessment documents the importance of addressing
risks associated with the widely occurring bacterium Listeria monocytogenes
(HHS/USDA, 2003). Listeriosis (the most serious illness induced by this
pathogen) occurs rarely (i.e., currently approximately 3.4 cases per million
people annually). When it does occur, however, it can be life threatening.
Two population groups (pregnant women and their fetuses and elderly and
other individuals who have a pre-existing illness that reduces the effectiveness
of their immune system) are especially susceptible to potentially life-threatening
human illness from listeriosis. In healthy people, the microorganism usually
causes only a noninvasive gastrointestinal illness, with symptoms including
fever, vomiting, and/or diarrhea (HHS/USDA, 2003).
Of the foodborne pathogens tracked by CDC, Listeria monocytogenes
had the second highest case fatality rate (21 percent) and the highest hospitalization
rate (90.5 percent). If a pregnant woman develops listeriosis, her fetus
also becomes exposed. Fetal infection can lead to fetal death, premature
birth, or neonatal illness and death. Other people with impaired T-cell
immunity (immunocompromised patients and elderly) also are especially vulnerable
to the high lethality of listeriosis (Rocourt et al., 2003).
Most prenatal cases of listeriosis are reported in the third trimester
(Slutsker and Schuchat, 1999). A few days after the onset of symptoms, a
pregnant woman may abort the fetus or have premature delivery (Gellin and
Broome, 1989). Late in the pregnancy, listeriosis may result in stillbirth
or birth of a critically ill newborn. Listeriosis in the first trimester
may result in spontaneous abortion.
Foods that pose high risk for listeriosis have all the following properties:
(1) relatively high rates of contamination with L. monocytogenes,
(2) characteristics that support the growth of L. monocytogenes
to high numbers when refrigerated, (3) ready-to-eat, and (4) commonly stored
for extended periods (HHS/USDA, 2003). Two food categories—deli meats (excluding
those that are very salty, such as some ham, or low in water activity, such
as hard salami) and frankfurters that have not been reheated to a safe temperature—have
been categorized as very high risk for listeriosis. According to
the Quantitative Assessment (HHS/USDA, 2003), this risk designation is consistent
with the need for immediate attention for reducing the incidence of foodborne
listeriosis. Addressing this risk in dietary guidance would be consistent
with the position of Medeiros and colleagues (2001a; 2001b) that food safety
education programs ensure that messages are aimed at reducing the risk of
the most prevalent and/or serious causes of foodborne illness.
A report from the International Life Sciences Institute (ILSI) Risk Science
Institute Expert Panel (2004) recommends that high-risk individuals (i.e.,
the elderly, pregnant women, and most immunocompromised people) should be
given specific information on high-risk foods that they should avoid, and
strategies to reduce their risk, such as thorough cooking, avoidance of
cross-contamination and short-term refrigerated storage of cooked, perishable
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Methylmercury in Fish
Methylmercury is a heavy metal toxin found in varying levels in different
types of fish. This toxin can cause neurological harm to fetuses and young
children, whose brains are still developing. Mahaffey and colleagues (2004),
using blood methylmercury data and fish intake data from the 1999–2000 National
Health and Nutrition Examination Survey, estimated in utero
methylmercury concentrations of newborns. They estimated that more than
300,000 U.S. newborns each year may have been exposed to methylmercury concentrations
higher than those considered to be without increased risk of adverse neurodevelopmental
effects. The FDA released an advisory in March 2004 (U.S Food and Drug Administration,
2004)) for women and young children, developed jointly with the Environmental
Protection Agency, that provides guidance on how to receive the benefits
of eating fish while being confident that exposure to the harmful effects
of mercury is very low. The advisory warns against eating shark, swordfish,
king mackerel, or tilefish because these fish contain high levels of mercury.
Instead, the advisory recommends that women eat up to 12 ounces per week
of a variety of fish and shellfish that are lower in mercury (e.g., shrimp,
canned light tuna, salmon, pollock, and catfish). Since albacore ("white")
tuna is commonly eaten and has more mercury than canned light tuna, women
are advised to limit their intake to 6 ounces of albacore tuna per week.
The advisory calls for smaller portions of these fish for young children.
Advice also is provided about fish from local waters.
Schober et al. (2003) found that measures of mercury exposure in women
of childbearing age and in young children generally fall below levels of
concern. They recommend that women who are pregnant or who intend to become
pregnant follow Federal and State advisories on consumption of fish. Because
of wide variations in the concentrations of mercury in different kinds of
fish and shellfish, it is possible to have the nutritional benefits of moderate
fish consumption and avoid fish high in mercury (Schober, 2003).
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Taking four basic food safety measures can help consumers protect against
foodborne illness. These measures include cleaning hands, contact surfaces,
and fruits and vegetables; separating raw, cooked, and ready-to-eat foods
while shopping, preparing, or storing; cooking foods to a safe temperature;
and chilling perishable foods promptly. In addition, avoiding higher risk
foods (such as frankfurters that have not been reheated to a safe temperature)
is an important protective measure, especially for high-risk groups (the
very young, pregnant women, the elderly, and those who are immunocompromised).
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