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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 250F 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 F250F 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 F250F of 2.45 min and a z of 17.6F (Townsend et al., 1938~. These values were generally rounded up to 3 min and 18F. 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 250F 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 F250F 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 14F and not 18F. 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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216 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 30C (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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220 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. REFERENCES AMS (Agricultural Marketing Service). 2001. Microbiological Data Program. What is MDP? Online. U.S. Department of Agriculture (USDA). Available at http://amsdev.ams.usda.gov/science/mpo/ what.htm. Accessed September 19, 2002. Becci PI, Hess FG, Johnson WD, Gallo MA, Babish JG, Dailey RE, Parent RA. 1981. Long-term carcinogenicity study of patulin in the rat. JAppl Toxicol 1:256-261. Besser RE, Lett SM, Weber IT, Doyle MP, Barrett TJ, Wells JG, Griffin PM. 1993. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia cold 0157:H7 in fresh-pressed apple cider. JAMA 269:2217-2220. Beuchat LR. 1998. Surface Decontamination of Fruits and Vegetables Eaten Raw: A Review. WHO/ FSF/FOS/98.2. Geneva: World Health Organization. Birkhead GS, Morse DL, Levine WC, Fudala JK, Kondracki SF, Chang HO, Shaydgani M, Novick L, Blake PA. 1993. Typhoid fever at a resort hotel in New York: A large outbreak with an unusual vehicle. J Infect Dis 167:1228-1232. Buchanan RL, Edelson SO, Miller RL, Sapers GM. 1999. Contamination of intact apples after immersion in an aqueous environment containing Escherichia cold 0157:H7. J Food Prot 62:444-450. Butler ME. 2000. Salmonella outbreak leads to juice recall in Western states. Food Chem News 42:19. CAC (Codex Alimentarius Commission). 2000. Draft Code of Hygienic Practices for Primary Production, Harvesting, and Packaging for Fresh Fruits and Vegetables. Rome: FAO. Pp.6-7. California State Board of Health. 1920. Resolutions of the California State Board of Health on the packing of ripe olives in California. Calif State Board Health Mon Bull 16:35. California Strawberry Commission. 1998. Quality Assurance Program. Watsonville, CA: California Strawberry Commission. CAST (Council for Agricultural Science and Technology). 2003. Mycotoxins: Risks in Plant, Animal and Human Systems. Task Force Report No. 139. Ames, IA: CAST. CDC (Centers for Disease Control and Prevention). 1975. Salmonella typhimurium outbreak traced to a commercial apple cider New Jersey. Morb Mortal Wkly Rep 24:87-88. CDC. 1995. Outbreak of SalmonellaHartford Infections among Travelers to Orlando, Florida. EPI-AID Trip Rpt. 95-62. Atlanta, GA: CDC. CDC. 1996. Outbreak of Escherichia cold 0157:H7 infections associated with drinking unpasteur- ized commercial apple juice British Columbia, California, Colorado, and Washington, Octo- ber 1996. Morb Mortal Wkly Rep 45:975. CDC. 1997. Outbreaks of Escherichia cold 0157:H7 infection and cryptosporidiosis associated with drinking unpasteurized apple cider Connecticut and New York, October 1996. Morb Mortal Wkly Rep 46:4-8. CDC. 1998. Botulism in the United States 1899Handbook for Epidemiologists, Clinicians and Laboratory Workers. Atlanta: CDC. CDC. 1999. Oubreak of Salmonella serotype Muenchen infections associated with unpasteurized orange juice United States and Canada, June 1999. Morb Mortal Wkly Rep 48:582-585.

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