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6
Scientific Criteria and
Performance Standards to Control Hazards
in Produce and Related Products
FRESH FRUITS AND VEGETABLES AND FRESH-CUT PRODUCTS
Background
Fruits and vegetables provide many health benefits and are an important
component of the American diet. People interested in lowering their consumption
of total calories, fats, and cholesterol, as well as in protecting against certain
types of cancer, are incorporating more fruits and vegetables into their diets.
The fresh fruit and vegetable industry experienced solid growth in the late
1990s, as evidenced by the increasing space devoted to these products in super-
markets and on restaurant menus throughout the United States (IFT, 2001~. This
growth is expected to increase in the future. As many industry and government
programs have promoted increased consumption of produce, consumers have
responded to these messages by increasing their consumption of fruits and veg-
etables from 284 pounds per capita in 1987 to 319 pounds in 1997 (Kaufman et
al., 2000~. Growers, in turn, have responded by producing a wide variety of
traditional and new fruits and vegetables. Because of advances in agronomic
practices, preservation technologies, shipping practices, and improved cold-chain
management, global production and distribution of fresh fruits and vegetables
have increased. Through innovative packaging systems and improved marketing
and merchandising strategies, consumers can choose from an average of 345
different produce items in a typical retail food store (Litwak, 1998~.
Imports of fresh fruits and vegetables also increased significantly as U.S.
food preferences and consumption patterns shifted. In 2001, U.S. imports of fresh
197
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98
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
fruits and vegetables were 38.3 percent and 13.3 percent, respectively, of the total
national consumption of these products (Personal communication, G. Lucier and
S.L. Pollack, U.S. Department of Agriculture, December 2002~. Increases in
global food trade have made produce from over 130 countries around the world
available to U.S. consumers and provide year-round availability of fresh produce
(Rangarajan et al., 1999~. Mexico is now the source of 27 percent of U.S. fruit
imports and 38 percent of vegetable imports (Jerardo, 2002~. Off-season fruit
imports from Chile and Argentina and vegetable imports from Peru, Ecuador, and
other South American countries are also driving up the overall U.S. import shares
of these commodities. Excluding Mexico, Latin American countries supply an
additional 40 percent share of U.S. imported fruits, the largest share being
bananas, grapes, and melons. It is not surprising that there is a seasonal pattern to
fresh vegetable imports, with two-thirds of the import volume arriving between
December and April when U.S. production is low and limited to the southern
growing regions of the country (ERS, 2002~.
A niche for fresh-cut fruits and vegetables was established in the 1980s and
its market has increased exponentially since then because of the demand for
convenience and value-added products by consumers, food retailers, and the
foodservice industry (IFT, 2001~. Fresh-cut produce is "any fresh fruit or vege-
table, or any combination thereof that has been physically altered from its origi-
nal form, but remains in the fresh state" (IFPA, 2001~.
While providing many health benefits, raw fruits and vegetables have also
been known for at least a century to be potential vehicles for human disease
(Beuchat, 1998~. In the late 1800s, one of the first reports of produce-associated
foodborne illness linked typhoid infection to eating celery (Morse, 1899~. Another
outbreak of typhoid fever was attributed to eating watercress grown in soil
fertilized with sewage (Warry, 1903), and two cases were attributed to eating
uncooked rhubarb grown in soil fertilized with typhoid excrete (Pixley, 1913~.
These and other early reports of microorganisms surviving on vegetables and
plant tissues (Creel, 1912; Melnick, 1917) demonstrated that raw fruits and veg-
etables could serve as vehicles for the transmission of human pathogens. While
fresh produce can serve as a source of all classes of foodborne pathogens (i.e.,
bacteria, viruses, protozoa, fungi, and helminths), pathogenic bacteria raise the
greatest concerns because the risk of illness they pose may be amplified by
potential growth prior to consumption (NACMCF, 1999a).
Although fresh fruits and vegetables have recently been associated with
foodborne disease outbreaks, these products were not thought to be common
causes of foodborne illnesses in the United States; instead, they were considered
to be relatively safe foods (NRC, 1985~. The acidity of many fruits was believed
to inhibit the growth and to decrease populations of human pathogens, while the
edible portions, protected from contamination by a skin or thick rind, were con-
sidered safe as well (NRC, 1985~. It was recognized, however, that produce
imported from countries where polluted water or raw sewage was used for irriga-
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
199
lion, fertilization, washing, cooling, or icing could be contaminated with enteric
pathogens and might be a potential source of foodborne illness. A report issued in
1985, An Evaluation of the Role of Microbiological Criteria for Foods and Food
Ingredients (NRC, 1985), addressed the need for microbiological criteria for
various food groups. With regard to fresh fruits and vegetables, this report made
the following statement: "there is little use for microbiological criteria for fresh
fruits and vegetables at the present time. However, future changes in irrigation
and fertilization practices in this country or changes in the source of imported
produce could mandate testing for certain pathogens or indicator organisms"
(NRC, 1985~.
In the past two decades, as consumers have increased their consumption of
fresh fruits and vegetables, there has also been a significant increase in the number
of foodborne disease outbreaks and cases associated with these foods. According
to the Centers for Disease Control and Prevention (CDC), foodborne disease
surveillance reports for the periods 1983 to 1987 and 1988 to 1992 suggest that
the annual number of reported produce-associated disease outbreaks, the number
of persons affected annually in those outbreaks, and the proportion of outbreaks
due to fresh produce among those illnesses with an identified food vehicle has at
least doubled (NACMCF,1999a). Outbreaks of foodborne illness associated with
produce in the United States for the period 1973 to 1997 are shown in Figure 6.1.
An in-depth analysis of published outbreak investigations by a panel of
experts (IFT, 2001) revealed that outbreak data has linked the following patho-
genic organisms with the consumption of specific produce commodities:
Clostridium botulinum with cabbage salad; Campylobacter jejuni with salad and
lettuce; Escherichia cold 0157:H7 with spring mix, lettuce, seed sprouts, and
cantaloupe; Listeria monocytogenes with cabbage salad; Shigella spp. with shredded
lettuce, parsley, and scallions; Salmonella spp. with seed sprouts, green onions,
tomatoes, melons, and mangoes; hepatitis A virus with tomatoes, lettuce, water-
cress, and frozen raspberries and strawberries; calicivirus with salad and frozen
raspberries; Norwalk virus with cut fruits; Cyclospora with raspberries, mesculun
lettuce, and basil and basil-containing products; and Giardia with lettuce and
onions (see Table 6.1~. There have also been outbreaks linking Cryptosporidium
and E. cold 0157:H7 with nonpasteurized apple cider, and Salmonella with
nonpasteurized orange juice (IFT 2001; NACMCF, 1999a).
Most of the identified fresh produce-associated disease outbreaks in the
United States from 1988 to 1998 were caused by bacteria, especially Salmonella
spp. and E. cold 0157:H7, and from 1990 to 1998, three-fourths of the reported
outbreaks were attributed to domestic produce (Personal communication, A.
Liang, CDC, 1999~. In addition to the produce-associated foodborne disease
outbreak statistics compiled and reported by CDC, the Center for Science in the
Public Interest (CSPI) also developed a database of foodborne outbreaks that
occurred in the United States between 1990 and 2001. CSPI (2001) reported that
148 outbreaks consisting of 10,504 cases (an average of 71 cases per outbreak)
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200
50
45
40
35
E 30
<,, 25
`t 20
15
10
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
~ Number of outbreaks
1111 Number of ill individuals
~-
1 970s
1 980s
Year
1 990s
FIGURE 6.1 Outbreaks of foodborne illness associated with fresh produce in the United
States, 1973-1997.
were associated with produce; vegetables were associated with 78 percent of
these outbreaks and fruits were associated with 18 percent. Five percent were
associated with both fruits and vegetables (CSPI, 20011.
Fresh produce safety is of special concern to the public health community
because fruits and vegetables do not receive any treatment specifically designed
to kill all microbial pathogens prior to consumption. Although the incidence of
foodborne illness linked to produce is still low, produce-associated illnesses erode
consumer confidence in the safety of fresh fruits and vegetables and cause con-
cern about the risk attributable to the consumption of these foods. There are still
many questions about the transmission of microorganisms from their potential
reservoirs to fruits and vegetables, including knowledge about any vectors that
may be involved in this process. While all produce items have risk factors in
common, it is important to recognize that each fruit and vegetable has a unique
combination of composition and physical characteristics, as well as growing and
harvesting practices, cooling techniques, and optimal storage temperatures under
which it is managed. Because of the lack of lethal treatments between farm
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
201
TABLE 6.1 Some Multistate Foodborne Disease Outbreaks Involving Produce
in the United States, 1994-2001
Number
Year Pathogen of States
Food Source
1994 Shigella J?exneri 2
1996 Cyclospora 20
cayetanesis
1996 Salmonella Infantis 2
1996 Escherichia cold
0157:H7
1996 E. cold 0157:H7
4
1997 C. cayetanesis 18
1997 Hepatitis A
1998- S. Baildon Multistate
1999
1998 S. sonnet
1999 S. Muenchen 20
1999 S. Mbandaka 4
2000 S. Enteriditis
2000 S. Newport
2001 S. Poona
Green onions, probably contaminated in Mexico
Raspberries from Guatemala (mode of
contamination unclear); cases were also
reported in the District of Columbia and two
Canadian provinces
Alfalfa sprouts, probably contaminated during
sprouting
Multistate
10
16
2 The implicated lettuce was traced to a single
grower processor; cattle was found near the
lettuce fields
U.S.-grown apples were phosphoric acid
washed, brushed, and rinsed; however,
phosphoric acid-based solutions may have
been used incorrectly (not intended for
produce/waxed produce) or sometimes used at
low concentrations; possibly poor quality
apples, some dropped apples used, apple
orchard near cattle/deer
Raspberries imported from Guatemala,
mesculun lettuce, and products containing
basil; cases were also reported in the District
of Columbia and two Canadian provinces
Strawberries from Mexico distributed through
the U.S. Department of Agriculture
Commodity Program for use in school lunches
Tomatoes traced to two packers in Florida;
possible field contamination by domestic or
wild animals
Imported parsley, probably contaminated during
washing after harvest
Unpasteurized orange juice produced in Mexico
and bottled in the United States
Sprout seeds were believed to come from the
same lot and distributed to various growers in
California, Florida, and Washington
Gallon-sized containers of domestic citrus juices
were implicated in the outbreak
Imported mangoes, likely contaminated during
treatment to kill fruit flies
Imported cantaloupe, probably contaminated in
the field or shortly after harvest
2002 S. Javiana 50 Tomatoes
2002 S. Newport 18 Tomatoes
SOURCE: IFT (2001).
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202
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
production and consumption, microbial pathogens introduced on fresh produce at
any point in the production and distribution chain may be present at the point of
consumption. Moreover, anything in the production environment that comes in
contact with the plant has the potential for being a source of pathogens. Although
the ultimate source of fresh produce contamination with most enteric pathogens
is animal or human fecal material, potential direct and indirect sources of con-
tamination from farm to table include soil; manure; irrigation water; wild and
domestic animals; farm, packinghouse, and terminal market workers; contami-
nated equipment; wash and rinse water; ice; cooling units; transportation vehicles;
cross-contamination from other food products; and improper storage, packaging,
and display (Beuchat, 1998; FDA/USDA/CDC, 1998; Rangarajan et al., 1999~.
The growth, survival, and inactivation of microorganisms on fresh fruits and
vegetables is dependent on the interaction of many factors; therefore, preventing
contamination of produce with microbial pathogens rather than removing them
at a later point is considered to be the most effective strategy in assuring the
safety of these foods (FDA/USDA/CDC, 1998; IFT, 2001~. Many effective inter-
vention strategies have been developed and implemented on farms and in packing-
houses but, as mentioned above, they cannot completely eliminate microbial
hazards potentially present on or in raw produce (IFT, 2001~. For these reasons,
to reduce the risk of produce-borne disease, the focus of intervention strategies
must be on preventing the introduction of biological, chemical, and physical
hazards into these products.
Current Criteria and Standards
J-
Unlike the dairy and seafood industry where microbial criteria and standards
have been in use for many years, there are virtually no criteria or standards for
microbiological safety currently being applied to fresh or fresh-cut produce by
U.S. federal government agencies other than those pertaining to sprouts and fruit
uices (discussed later in this chapter).
To minimize foodborne disease from being transmitted through fresh produce,
it is necessary to prevent initial contamination of these products and to control the
potential amplification of pathogens in them throughout the production and dis-
tribution chain. Intervention strategies currently being applied in the fresh produce
industry are Good Agricultural Practices (GAPs) in the field and packinghouses
(FDA/USDA/CDC, 1998) and Good Manufacturing Practices (GMPs) in fresh-
cut operations (21 C.F.R. part 110~. GAPs are similar to the GMPs used by food
processors, but GAPs address agricultural activities, including preplanting, plant-
ing, harvest, and postharvest practices that are designed to reduce microbial risks.
Several guidance documents that address GAPs have been developed and
widely disseminated by government agencies, growers, shippers, processor trade
associations, and academia (IFPA, 2001~. Some of these publications include the
Voluntary Food Safety Guidelines for Fresh Produce, published by the Inter-
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
203
national Fresh Cut Produce Association (IFPA) and the Western Growers Asso-
ciation (IFPA, 1997~; the Quality Assurance Program of the California Straw-
berry Commission (1998~; the Food and Drug Administration (FDA) guidance
document, Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits
and Vegetables (FDA/USDA/CDC, 1998~; and Food Safety Begins on the Farm,
from Cornell University (Rangarajan et al., 1999~. The FDA guidance document
describes eight areas in the growing and handling of produce where microbial
contamination may occur; it also urges growers to be aware of the potential for
contamination and to manage their operations in ways that minimize that potential
(FDA/USDA/CDC, 1998~. This document sets forth eight principles of microbial
food safety that can be applied to the growing, harvesting, packing, and transpor-
tation of fresh fruits and vegetables, as follows:
1. The prevention of microbial contamination of fresh produce is favored
over reliance on corrective actions once contamination has occurred.
2. To minimize microbial food safety hazards in fresh produce, growers or
packers should use GAPs in those areas over which they have a degree of
control while not increasing other risks to the food supply or the environ-
ment.
3. Anything that comes in contact with fresh produce has the potential of
contaminating it. For most foodborne pathogens associated with produce,
the major source of contamination is human or animal feces.
4. Whenever water comes in contact with fresh produce, its source and
quality dictate the potential for contamination.
5. Agricultural practices using manure or municipal biosolid wastes should
be closely managed to minimize the potential for microbial contamination
of fresh produce.
6. Worker hygiene and sanitation practices during production, harvesting,
sorting, packing, and transportation play a critical role in minimizing the
potential for microbial contamination of fresh produce.
7. Follow all applicable local, state, and federal laws and regulations, or
corresponding or similar laws, regulations, or standards for agricultural
practices for operators outside the United States.
8. Accountability at all levels of the agricultural environment (farms, packing
facility, distribution center, and transport operation) is important to a
successful food safety program. There must be qualified personnel and
effective supervision to ensure that all elements of the program function
correctly and to help track produce back through the distribution channels
to the producer.
The committee recognizes that the principles that make up the current GAP
recommendations are necessarily general given the broad range of fruits and
vegetables and their growing conditions and, like GMPs, they focus on minimiz-
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204
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
ing the potential for microbial contamination. In the case of GAPs, these prin-
ciples focus on prevention of contamination primarily from fecal material, water
sources, application of manure or biosolids, or poor personal hygiene.
The committee also recognizes that data on risks associated with many
specific practices in the fresh produce sector are lacking, so it is difficult to assess
which intervention strategies are necessary and which will provide the greatest
reduction in risk. Research in this area has been very active in recent years;
therefore, it is expected that data from such research will provide the necessary
information to supplement the basic guidelines.
In addition to the use of GAPs to minimize the probability of microbial
contamination of fruits and vegetables, some produce buyers have introduced
purchasing specifications; letters of guarantee; vendor certification programs;
and independent, third-party audits to provide assurance that growers are follow-
ing GAPs (IFPA, 2001; IFT, 2001~.
A unique feature of fruits and vegetables is that although microbial contami-
nation is most often associated with their surfaces, the interior tissues of solid
produce have been traditionally considered to be sterile. However, an early study
reported that the application of bacteria to the surface of fruits could result in their
internalization over time (Samish and Etinger-Tulczynska,1963~. Later, a number
of researchers reported isolating low levels of bacteria from internal tissues of
intact vegetables or radish sprouts (Lund, 1992; Robbs et al., 1996~. Other
research findings suggest that E. cold 0157:H7 in irrigation water and manure can
be internalized into lettuce plant tissue (Solomon et al., 2002), but the design of
this study did not reflect typical lettuce growing conditions.
The committee, aware of the importance of the issue of internalization of
pathogenic bacteria during growth or processing of produce, recommends that
FDA conduct or support additional studies to determine whether the internaliza-
tion of bacteria represents a significant safety hazard in fruits and vegetables.
A more widely recognized fact is that if flume or dump-tank water is cold
and contaminated with pathogens and warm fruit (e.g., apples or tomatoes) is
immersed in it, the pathogens can be internalized (Buchanan et al., 1999; Rushing
et al., 1996; Zhuang et al., 1995~. This led to the recommendation that flume
water for certain commodities be treated with an appropriate antimicrobial agent
such as chlorine, and that it be warmer than the incoming product (FDA/USDA/
CDC, 1998~.
Although the Hazard Analysis and Critical Control Point (HACCP) system
has long been recognized as the most effective and flexible system for assuring
the microbiological safety of a variety of foods, there have been few attempts to
integrate the various steps associated with the production and processing of fresh
produce into a farm-to-table HACCP system. Several HACCP plans have been
developed for sprouted seeds, shredded lettuce, and tomatoes (Rushing et al.,
1996), but complete validation of these plans has not yet been accomplished
(NACMCF,1999b). Available data are insufficient to develop validated HACCP
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
205
plans for most fresh produce items. Also, prerequisite programs, such as GAPs
and GMPs, which provide the foundation for HACCP systems, are still being
defined and evaluated for their effectiveness on farms and in orchards.
As the trend toward greater importation of fruits and vegetables into the
United States increases, there are concerns about the harmonization of food safety
standards for imported produce (IFT, 2001~. Several efforts are currently under-
way to harmonize these standards. In addition to the FDA guidance document
(FDA/USDA/CDC, 1998), the Codex Alimentarius a joint program of the Food
and Agriculture Organization of the United Nations (FAO) and the World Health
Organization (WHO) through its Committee on Food Hygiene, is developing
standards for the production of fresh produce, fresh-cut produce, and sprouts
(CAC, 2000~. This code of practice, similar to the FDA guidance document in
that it stresses prevention strategies for growers, is undergoing the Codex
Alimentarius comment process for approval.
Recently, FDA collected and analyzed selected samples of imported and
domestic produce to determine the incidence of microbial contamination on these
commodities. This project was undertaken to gather more data on the incidence
and extent of pathogen contamination of fresh produce and to assist the agency in
the development of policy for the Produce Safety Initiative (OPDFB, 2001~. A
total of 1,003 imported fruit and vegetable samples from 21 countries were col-
lected and analyzed. Of these, 4.4 percent tested positive for either Salmonella or
Shigella, whereas no products were positive for E. cold 0157:H7 (OPDFB,2001~.
In the domestic survey, FDA sampled and analyzed 767 commodities of which
1.6 percent tested positive for pathogens; specifically, 0.8 percent (6 samples)
were positive for Salmonella and an equal percentage were positive for Shigella
(CFSAN, 2001~.
In addition to FDA's surveillance efforts, the U.S. Department of Agriculture,
through its Agricultural Marketing Service (AMS), began a cooperative federal/
state effort in 2000 to establish a microbiological baseline to assess the risk of
contamination in the domestic food supply. As part of this Microbiological Data
Program, AMS is collecting retail samples of selected domestic and imported
fruits and vegetables to assess the incidence, number, and species of important
foodborne pathogens and indicator organisms present in them (AMS, 2001~. The
information obtained from the data program will be used to establish "bench-
marks" for evaluating the efficacy of procedures to prevent or reduce contamina-
tion of fresh fruits and vegetables with harmful microorganisms (AMS, 2001~.
FRUIT AND VEGETABLE,JUICES
Background
Similar to whole fruits, fruit juices were historically considered to present
minimal risks to health. This belief was derived from the expected inhibitory
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206
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
TABLE 6.2 Foodborne Disease Outbreaks Associated with Consumption of
Reconstituted Frozen Orange Juice Prior to 1990
Pathogen Year Location Venue Cases Reference
Salmonella 1944 Ohio Residential 18, 1 death Duncan et al., 1946
Typhi hotel
Hepatitis A 1962 Missouri Hospital 24 Eisenstein et al., 1963
Unknown 1965 California Football game 563 Tabershaw et al., 1967
S. Typhi 1989 New York Resort hotel 46 confirmed, Birkhead et al., 1993
24 suspected
properties of high organic acid levels, and consequent low pH, on bacterial
growth, and from the fact that most juices undergo a thermal process. In fact,
documented foodborne illnesses were rare (NRC, 1985~. In the early 1990s,
increased interest in raw fruit juices and improvements in cold distribution sys-
tems led to an increase in the processing and distribution of raw, nonpasteurized
fruit juices. Many of the foodborne disease outbreaks attributable to juices that
had occurred in the United States prior to 1990 were caused by asymptomatic
human handlers (workers shedding pathogens in their feces without showing
signs of illness) who contaminated orange juice with hepatitis A or Salmonella
Typhi as the juice was being reconstituted at a food service establishment (see
Table 6.2~. In one outbreak, the source of contamination was thought to have
been the water used to dilute the concentrate (Tabershaw et al., 1967~. Outbreaks
associated with single-strength raw citrus juices prepared in large commercial
processing facilities were identified in the mid 1990s. In one outbreak implicat-
ing orange juice, toads in the orange groves were thought to be the source of
Salmonella, while a general lack of sanitation in the plant was thought to have
contributed to the extent of the outbreak (Cook et al., 1998; Parish, 1998~. Like-
wise, foodborne disease outbreaks implicating raw apple juice were uncommon
prior to the 1990s. However, beginning in 1991, several outbreaks associated
with E. cold 0157:H7 or with the protozoan parasite, C. parvum, were identified
(IFT,2001~. Table 6.3 describes some outbreaks of foodborne disease associated
with raw juices. Although early outbreaks were associated with small cider mills,
an outbreak was associated with a large commercial juice processor in 1996.
Lack of sanitation, coupled with the use of wind-fallen or dropped apples, im-
proper or no washing of the fruit prior to pressing, and proximity of cattle or deer
(reservoirs for the pathogens) were thought to have contributed to these out-
breaks.
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
TABLE 6.3 Selected Outbreaks of Foodborne Disease Associated with Raw
Apple or Orange Juices
207
Pathogen Juice Year Location Cases Reference
Salmonella Apple 1974 New Jersey 296 CDC, 1975
Typhimurium
Escherichia cold Apple 1991 Massachusetts 23 Besser et al., 1993
0157:H7
Cryptosporidium Apple 1993 Maine 160 primary, Millard et al., 1994
parvum 53 secondary
S. Gaminera, Orange 1995 Florida 63 ill, CDC, 1995;
S. Hartford, and 7 hospitalized Cook et al., 1998;
S. Rubislaw Parish, 1998
C. parvum Apple 1996 New York 20 confirmed, CDC, 1997
11 suspected
E. cold 0157:H7 Apple 1996 Connecticut 14 CDC, 1997
E. cold 0157:H7 Apple 1996 British 70, 1 death CDC, 1996;
Columbia, Cody et al., 1999
California,
Colorado, and
Washington
S. Muenchen Orange 1999 United States 207 confirmed, CDC, 1999
and Canada 91 suspected,
1 death
S. Enteriditis Orange 2000 Multistate 14 Butler, 2000
Current Criteria and Standards for juices
Pathogen Reduction
As a consequence of larger outbreaks associated with raw juices processed at
commercial facilities, FDA introduced regulations in 1998 and 2001 for all juices
produced for inter- or intrastate sale (CFSAN, 1998; FDA, 2001~. Subpart A of
the regulation (21 C.F.R. part 120) mandates that juice be produced under a
HACCP plan that has supporting GMPs and Sanitation Standard Operating Pro-
cedures. The sanitation procedures must, at a minimum, address monitoring and
record-keeping for eight specific points: (1) water safety, (2) cleanliness of food
contact surfaces, (3) cross-contamination, (4) hand washing and toilet facilities,
(5) adulteration, (6) labeling and use of toxic compounds, (7) employee health,
and (8) pest control.
Subpart B of the regulation requires that juice processors achieve at least a
5-D reduction (referred to as a 5-D process) of the pertinent microorganism,
which is defined as "the most resistant microorganism of public health signifi-
cance that is likely to occur in the juice." The identification of this microorganism
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214
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
The Scientific Basis for Criteria
The initial published work used to establish thermal processes in canned
foods is generally acknowledged to have been that of Esty and Meyer (1922~.
These researchers, using the limited bacteriological techniques available at the
time, described the heat resistance of suspensions of 109 strains of Bacillus
botulinus (now Clostridium botulinum) spores in phosphate buffer at tempera-
tures above boiling. Of greatest significance was the development of a thermal
destruction curve for a suspension of 60 billion spores of three of the most heat-
resistant isolates. More than 1,800 small glass tubes were filled with 2 mL of the
spore suspension and sealed. Multiple tubes were subjected to each of five tem-
peratures for various lengths of time. After heating, the tubes were opened and
the heated spore suspension was placed in nutrient medium, incubated for an
appropriate period, and then analyzed for the presence of growth. The minimum
time required to destroy this population of cells at each temperature was thus
determined. Esty and Meyer made the significant observation that the data were
logarithmic in the temperature range they evaluated. These data were later used to
calculate that a thermal process at 250°F for 2.78 min (sometimes rounded up to
3.0 min and known as the F value) would eliminate a population of 6 x 10~°
spores (theoretically, a 10.8-D process). This F250°F value and the calculated
z value (the temperature difference required to change the F value by 1 logic) was
generally used by the canning industry to establish equivalent processes at other
temperatures. Esty and Meyer were attempting to achieve maximum levels of
spore populations in their preparation that, in other experiments, ranged from
1 x 106 to 1 x 109. The level of 6.0 x 10~° used in their classic experiment appears
to have been simply a level that they were able to achieve with this particular
spore preparation. These data were later confirmed and, after introducing correc-
tions for heating time, modified to an F250°F of 2.45 min and a z of 17.6°F
(Townsend et al., 1938~. These values were generally rounded up to 3 min and
18°F.
In 1950, Stumbo and coworkers published the first methods for determining
and calculating D values for C. botulinum. The D value is the time required to
destroy 90 percent of the cells in a suspension and, unlike the F value, it is not
dependent upon the initial spore load. The D value for C. botulinum 62A in
phosphate buffer at 250°F was reported to be 0.133 min by Stumbo and col-
leagues (1950) and 0.2 min by Schmidt (1964~. By dividing Schmidt's D value of
0.2 into the F250°F value of 2.45 minutes of Townsend and colleagues (1938), a
12.25-D process was estimated. It is not clear whether this is the true origin of the
accepted, but rather arbitrary, 12-D process; nevertheless, it appears to be an
approximate account of how the scientific information evolved (Perkins, 1964;
Stumbo, 1973~. Stumbo (1973) noted that, with an estimated 1 spore per can of
C. botulinum, this process results in a product for which the probability of this
microorganism surviving is 1 in 1 trillion cans. Stumbo and coworkers (1975)
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
215
later argued that a target of 1 viable spore in no more than 1 trillion cans should
be determined using the following assumptions: that C. botulinum spores might
be present at 1/g of food, and that the z value used to calculate the thermal
processes should be 14°F and not 18°F. Their calculated thermal processes were,
therefore, greater than those commercially applied at the time, particularly for
larger can sizes where a 15-D process needed to be applied (due to an estimated
thousands of cells per can) and at lower processing temperatures. Pflug and
Odlaug (1978) challenged the assumptions of Stumbo and coworkers, arguing
that a target of 1 viable spore in no more than 1 billion cans was adequate
protection of public health. They also maintained that the epidemiological evi-
dence supported the less conservative approach. They evaluated six outbreaks of
botulism occurring from commercially processed canned foods between 1963
and 1974. All were attributed to the use of an incorrect process, a failure to
deliver the scheduled thermal process, or postprocess contamination, and not to
inadequate assumptions used to calculate the process (Pflug and Odlaug, 1978~.
Adequate training of personnel in the canning facility was emphasized as critical
to the further reduction of botulism from commercially canned foods.
The D-value concept is still widely used to calculate thermal processes.
However, the basic assumption that thermal inactivation of microbial spores or
vegetative cells follows first-order kinetics (is linear) has recently been chal-
lenged (Peleg and Cole, 1998; van Boekel, 2002~. This is particularly problem-
atic when thermal death times are calculated by extrapolation. Although the use
of the 12-D thermal process has a long history of safe use, its appropriateness
should be scientifically reevaluated.
Technological innovations, through the use of alternative food-processing
technologies (including microwave and radio frequency processing, ohmic and
inductive heating, high pressure processing, pulsed electric fields, high voltage
arc discharge, pulsed light technology, oscillating magnetic fields, ultraviolet
light, ultrasound, and pulsed X-rays), are critical to the development of new fruit
and vegetable products and the reduction and inactivation of pathogens of public
health significance. As research and development continue to determine the
efficacy of these processes for a variety of foods, it is important to recognize that
any performance standards for these technologies require the following actions:
(1) the use of pathogens most resistant to the technology, (2) a description of the
mechanism of pathogen inactivation and its kinetics, (3) a determination of
mechanisms to validate the effectiveness of microbial inactivation, (4) the identi-
fication of critical process factors, and (5) a description of the process deviations
and corrective actions. Guidance must be provided by the agency on ways to
validate the process. When assessing any nonthermal process for shelf-stable
foods, the selection of an appropriate performance standard should be evaluated
on scientific merit. Many thermal processes far exceed the 12-D process for
C. botulinum in order to eliminate spoilage spores of microorganisms of greater
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SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
heat resistance, a fact that is likely to hold true of nonthermal processes (Stumbo,
1973~.
It is generally accepted that C. botulinum will not grow and produce toxin in
foods having pH values of 4.6 or below (Kim and Foegeding, 1992~. Dozier
(1924) published the first comprehensive study on this topic, followed by
Townsend and coworkers (1954~. Both noted that a pH of 4.8 to 4.9 was the
minimum for botulinal growth and toxin production in food. Since then, there
have been a number of reports of C. botulinum growth and toxin production in
laboratory media at pH values lower than 4.6 (Tanaka, 1982; Young-Perkins and
Merson,1987~; however, media with high protein concentrations were necessary
for growth and for toxin development to occur. The levels of protein in fruits and
vegetables have not been shown to support the growth of C. botulinum at pH
values lower than 4.6 (Kim and Foegeding, 1992~. Outbreaks of botulism in acid
foods are not entirely unknown (Odlaug and Pflug, 1978), but almost all have
been associated with underprocessed, home-canned foods where it is suspected
that surviving microorganisms may have altered the pH of the product, thus
allowing C. botulinum to grow. Adequate acidification and thermal processes, as
required by 9 C.F.R. part 114, should be sufficient to prevent botulism in these
products.
SPROUTS
As a result of several disease outbreaks associated with the consumption of
sprouts, FDA published a guidance document recommending that sprout producers
proceed as follows: (1) grow source seed under GAPs, (2) store seeds under
conditions that minimize contamination potential, (3) follow GMPs as per 21
C.F.R. part 110, (4) apply an appropriate seed treatment designed to reduce
pathogens (such as 20,000 ppm calcium hypochlorite), (5) sample and test sprout
irrigation water for Salmonella and E. cold 0157:H7, and (6) develop and imple-
ment systems to facilitate trace-back and recall (CFSAN, 1999~. Sprouts not
produced using the guidance document can be considered adulterated under the
Food, Drug, and Cosmetic Act. FDA issued a second document, also in 1999,
expanding on some of the decontamination measures recommended in the first
guidance document (NACMCF, l999b).
PESTICIDE RESIDUES
Under the Food Quality Protection Act of 1996, the U.S. Environmental
Protection Agency (EPA) must ensure that, before registering a new pesticide, it
can be used with a reasonable certainty of no harm to human health and the
environment. To determine its safety, more than 100 scientific studies and tests
are required from the applicants, from which EPA sets tolerance levels (maxi-
mum pesticide residue levels) for residues in the food. The applicant provides
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
217
information on the chemistry, safety, and tolerance of the new pesticide. In this
way, in addition to environmental effects, long- and short-term potential human
risks are evaluated. Pesticides are registered for use on specific crops.
Several factors must be addressed before a tolerance can be established, such
as the aggregate exposure to the pesticide, the cumulative effects from pesticides
with similar effects, increased susceptibilities of certain populations, and endo-
crine disrupter effects. These data are collected from industry as well as from
state and federal monitoring programs. EPA then develops a comprehensive risk
assessment (see Chapter 3 for a general description of the chemical risk assess-
ment process) to determine the impact of the affected crops on the safety of the
population and the environment. The risk assessment is then carefully reviewed
by scientific experts and a decision is made to approve or reject the pesticide. For
pesticides that are used in foods, EPA sets a tolerance, and FDA tests domestic
and imported produce to verify compliance. Other FDA programs are designed to
develop statistically valid information on pesticide residues that is used by EPA
in its risk assessments for pesticides in foods.
The committee believes that the process to establish pesticide tolerances in
produce is a good approach to ensure public health. The process of setting pesti-
cide tolerances by EPA is in agreement with the committee's belief that food
safety standards should be developed based on a combination of the best avail-
able science and expert opinion, and that this process should be a transparent one.
FOOD DEFECT ACTION LEVELS
The need to establish some type of defect levels for fruits and vegetables was
recognized soon after passage of the 1906 Federal Food and Drug Act (Merrill
and Hutt, 1980~. Defect Action Levels were established by FDA as maximum
levels of natural or unavoidable defects in foods for human use that present no
health hazard (CFSAN, 1998~. (See Appendix D for Defect Action Levels for
selected fruits and vegetables.)
Some foods, even when produced under GMPs, contain natural or unavoid-
able defects that, at low levels, are not hazardous to health. Even with current
technology, it is considered impractical or nearly impossible to produce foods
entirely free of natural or unavoidable defects. FDA has established maximum
levels for these defects in foods produced under current GMPs and uses these
levels to decide whether to recommend regulatory action. The agency makes it
clear in 21 C.F.R. part 110, subpart G. that "Defect action levels are established
for foods whenever it is necessary and feasible to do so. These levels are subject
to change upon the development of new technology or the availability of new
information."
Compliance with defect action levels does not excuse violation of the statu-
tory requirement (21 U.S.C. §402(a)~4~) that food not be prepared, packed, or
held under unsanitary conditions or the regulatory requirements (21 C.F.R. part
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218
SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
110) that food manufacturers, distributors, and holders shall observe GMPs. Evi-
dence indicating that such a violation exists causes the food to be adulterated,
even though the amounts of natural or unavoidable defects are lower than the
currently established defect action levels. FDA recommends that food manufac-
turers, distributors, and holders utilize quality control operations that reduce
natural or unavoidable defects to the lowest level currently feasible.
INTERNATIONAL CRITERIA
There are various published international criteria that are applied to produce,
as can be seen in Appendix E. However, there are a number of issues that make
the value of these criteria difficult to interpret. First, they are applied at different
stages, ranging from manufacturing, to retail, to the point of entry of imported
produce into a country, or at unspecified points. For example, the point of
application of standards for vegetables is either at the end of shelf-life, retail, or
not specified, in France, Ireland, and Spain, respectively. Second, the legal status
of these criteria mandatory or guidance is not specified. It is also unclear
whether any of these criteria are being enforced and, if they are, whether they are
effective or are being evaluated. In addition, there seem to be no organized efforts
to harmonize these standards among nations or within international organizations.
The usefulness and scientific basis of some of these criteria with regard to
public health can sometimes be questioned. For example, in Ireland there are
criteria for Vibrio parahaemolyticus in dried fruits and vegetables and for
Campylobacter in coleslaw, while Spain has criteria for L. monocytogenes in
canned raw vegetables. Other examples of questionable produce safety criteria
are a 200 cfu/g limit for nonpathogenic Listeria spp. in coleslaw, and a limit of
106 cfu/g of aerobic bacteria in mixed, prepared salads held at 30°C (see Appen-
dix E).
DO PRODUCE AND JUICE PERFORMANCE STANDARDS
IMPROVE PUBLIC HEALTH?
Tools for measuring the impact of food safety criteria on public health include
public health surveillance of several types, special studies, and outbreak investi-
gations (see Chapter 2~. These activities can help define the burden of disease
associated with specific pathogens and food groups, and can also serve to monitor
the effectiveness of control programs. Because of the complexity of foodborne
diseases, the effectiveness of these criteria is usually inferred, rather than directly
demonstrated; nonetheless, basic public health surveillance offers a final check
on the progress made in preventing foodborne diseases.
The committee recognizes that a clear example of the success of a perfor-
mance standard is illustrated by the fact that after the establishment of the low-
acid and acidified canned food rules and GMP regulations in the 1970s, only
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CONTROLS FOR HAZARDS IN PRODUCE AND RELATED PRODUCTS
219
occasional cases of botulism attributable to these foods have occurred. The com-
mittee also believes that although the 12-D performance standard for low-acid
canned foods might be too stringent in that it might compromise some quality
attributes of certain canned foods, and therefore requires scientific reevaluation,
the success of these criteria is nevertheless unquestionable.
Regarding the new juice regulations and sprouts guidance, the committee
considers that it would be premature to try to evaluate their public health impact,
for they were established just a few years ago. However, the fact that no disease
outbreaks attributable to Salmonella or E. cold 0157:H7 in juices have been
reported to CDC since the juice regulation was implemented is noteworthy. In
addition, all sprout outbreaks reported since the publication of the FDA guide-
lines have been associated with seed that was sanitized using methods other than
those described in the guideline.
Likewise, industry guidance documents such as GAPs have recently been
published and, therefore, although they are obviously valuable food safety tools,
information on their use and possible impact is not yet available. For example,
efforts to reduce the potential contamination of lettuce by water in hydrocoolers
may have reduced the number of outbreaks. The committee believes that although
the number and size of foodborne disease outbreaks associated with specific fresh
produce or juice items will, in the future, offer a means of tracking progress in
prevention, attributing changes in disease incidence to any specific factor con-
tinues to be a challenge because multiple confounding factors and safety measures
are being implemented in parallel.
The committee reiterates its belief that, because of the multiple confounding
factors, there is a need to develop a framework that allows for the timely sharing
of data from surveillance programs on microbial contamination in specific food
groups (in this case, fresh and fresh-cut produce and related products such as
juices) and from human, animal, and environmental isolates, as well as eventual
integration of such data. This framework, in addition to providing information for
risk assessments and allocating the burden of disease among specific commodi-
ties, could also be used to monitor the progress, over time, of particular microbio-
logical criteria in preventing the presence of hazardous levels of pathogens or
toxins in produce (see Chapter 2~.
The committee points to the need for a structured review process for guid-
ance documents and regulations, with input from a wide variety of experts from
industry, government, and academia, using the NACMCF model. This review
process should be used to modify or rescind criteria as science evolves. For issues
where the science is rapidly evolving (e.g., fresh produce, sprouts, juice) the
review process should take place on a more frequent basis than in areas of relative
scientific stability (e.g., thermally processed, low-acid canned foods). In all cases,
and to facilitate the review process, the scientific justification for published guid-
ance or regulations should be transparent and readily available, particularly when
the data are limited.
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SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD
The committee is aware that technological innovation based on nonthermal
food-processing technologies is critical to the development of new fruit and
vegetable products. However, the committee reiterates its recommendation that,
prior to developing performance standards that accommodate process or other
technical innovations, guidance must be provided to industry on process
validation.
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Representative terms from entire chapter:
fresh fruits
