While produce quality can be judged by outward appearance based on such criteria as color, turgidity, and aroma, food safety cannot. Casual inspection of produce cannot determine if it is in fact safe and wholesome to consume. Most fresh fruits and vegetables are grown in nonsterile environments, and conventional fruit and vegetable growers have less control over conditions in the production field as compared to an enclosed production or food preparation facility. The surfaces of produce have natural microflora composed of microorganisms that are generally benign. However, low-level contamination of produce with pathogenic microorganisms may sporadically occur. Production, harvesting, washing, cutting, slicing, packaging, transporting, and preparation all offer opportunities for produce contamination. While it is well established from the data presented above that the vast majority of produce contamination with human pathogens occurs in postproduction situations (Figure 1.1), if contamination does occur during growing and initial postharvest handling of produce, the consequences can be far greater. This is due to the potential for amplification of human pathogens throughout distribution and the increased risk of cross contamination posed by handling a food product contaminated with a human pathogen.
1.5.1 Food Safety Risk Factors Associated with Production of Fresh Produce
Management of growing conditions is of paramount importance in preventing the contamination of fresh produce by human pathogens. There are risk factors to consider such as growing conditions, agricultural practices used by specific growers, the time of year, growing region/environment, and management practices that may change over the course of a season. Climate, weather, water quality, soil fertility, pest control, as well as irrigation, and other management practices are difficult to integrate towards the development and implementation of microbial risk prevention and reduction programs on the farm .
Organic foods including organic fresh fruits and vegetables are one of the fastest-growing segments of the U.S. food industry, and there are many product claims among organic producers and handlers that organic products are safer and more nutritious. Only a limited number of studies have been conducted comparing conventional versus organic fruit and vegetable production practices and the effects on product food safety risk. There is currently no scientific evidence to support claims that organically grown fruits and vegetables are either safer or pose a greater food safety risk than conventionally grown produce [17-19].
The safety of fruits and vegetables grown on any given piece of land is not only influenced by the current agricultural practices but also by former land use practices. Human pathogens may persist in soils for long periods of time [20-22]. There may be increased risk of soil contamination if production land was previously used as a feedlot or for animal grazing since fecal contamination of the soil may be extensive. However, it is difficult to determine exactly the magnitude of the risk as the persistence of human pathogens in soil varies by the pathogen in question, soil type, climate, irrigation regimes, initial pathogen population numbers, etc. .
Soil amendments are commonly but not always incorporated into agricultural soils used for fruit and vegetable production to add organic and inorganic nutrients to the soil as well as to reduce soil compaction. Human pathogens may persist in animal manures for weeks or even months [24,25]. Proper composting via thermal treatment will reduce the risk of potential foodborne illness. However, the persistence of many human pathogens in untreated agricultural soils is currently unknown and under extensive investigation [26-28].
Wild and domestic animals such as birds, deer, dogs, rodents, amphibians, insects, and reptiles are known to be potential reservoirs for human pathogens and their feces may facilitate the spread of human pathogens in agricultural production settings, packinghouses, processing, and during distribution [29-31]. Food processing, warehousing, and distribution facilities routinely have animal control programs in place to prevent contamination of fruits and vegetables. However, production agriculture in open fields is challenged by infestation of wildlife and has only a limited number of remedies available to deal with periodic infestations by these pests. There is little or no data available for production agriculture operations to assess the risks associated with the presence of a particular wild animal species in production fields, field harvesting equipment, and/or in an adjacent field. While a zero tolerance for the presence of wild animals in production environs would potentially eliminate the risk of produce contamination, such operating procedures are simply impractical if not impossible to implement.
Irrigation water is another potential vector by which contaminants may be brought in contact with fruits and vegetables. Well water is perceived to be less likely to be contaminated with human pathogens than surface water supplies, due to the limited access to sources of potential contamination. Production agriculture operations routinely test irrigation water sources for the presence of human pathogens and/or indicator microorganisms. However, such testing is of only limited value, particularly for flowing surface water sources, since water tested at any given point in time will not necessarily be the same water used to irrigate crops in the future. Whenever water comes in direct contact with edible portions of fruits and vegetables, particular care should be taken to ensure that the water does not contain human pathogens. Pesticide application with contaminated water is thought to be the cause of the 1996 cyclosporosis outbreak associated with fresh raspberries grown in Guatemala [32-34], and recent research has demonstrated that commonly used pesticides and fungicides do not significantly affect the survival or growth of human pathogens .
Irrigation water if contaminated with human pathogens may contaminate soils, and splashing of soils by irrigation or heavy rain may facilitate produce contamination . A number of recent studies have also indicated that fresh produce may be contaminated by root uptake of human pathogens during irrigation with contaminated water [37,38]. Other research reports have indicated that this phenomenon does not occur [39,40]. It is currently unclear if root uptake of human pathogens is a significant source of contamination of fresh produce. However, direct contact of contaminated water with edible potions of crops is an obvious means of produce contamination by human pathogens.
During harvesting operations field personnel may contaminate fresh fruits and vegetables by simply touching them with an unclean hand or knife blade. Portable field latrines as well as hand wash stations are routinely made available and used by harvest personnel. Monitoring and enforcement of field worker personal hygiene practices such as hand washing after use of field latrines are critical to reduce the risk of human pathogen contamination on fresh produce. Due to the potential for contamination, produce once harvested should not be placed on bare soils before being placed in clean and sanitary field containers . Field harvesting tools should be clean, sanitary, and when possible not be placed directly in contact with soil. Harvest ladders are commonly used to harvest tree fruit and may serve as a potential source of contamination, if soiled ladder rungs are handled by pickers to move the ladder. Therefore, ladders should be constructed in a sanitary manner so as to allow the easy movement of the ladder without the fruit picker having to grip the ladder rungs. Reusable field harvest containers must also be cleaned and sanitized on a regular basis to reduce the potential for cross contamination.
1.5.2 Food Safety Risk Factors Associated with Postharvest Handling of Produce
Depending upon the commodity, produce may be field packaged in containers that will go all the way to the destination market or may be temporarily placed in bulk bins, baskets, or bags that will be transported to a packing shed. Employees, equipment, cold storage facilities, packaging materials, and any water that directly or indirectly contacts harvested produce must be kept clean and sanitary to prevent contamination.
Human beings are a significant reservoir for human pathogens and therefore gloves, hairnets, and clean smocks are routinely worn by packinghouse employees and field harvest crews to reduce the potential for contamination of fresh produce during handling. The cleanliness and personal hygiene of employees handling produce at all stages of production and handling must be managed to minimize the risk of contamination. Availability of adequate restroom facilities and hand washing stations and their proper use are critical to preventing contamination of produce by employees. Shoe or boot cleaning stations may also be in place to reduce the amount of field dirt and potential contamination from field operations that may enter packing sheds, processing plants, and distribution centers. Employee training regarding sanitary food handling practices, in a language in which employees are fluent, is essential to reducing the potential for employees contaminating food products that they are handling. This is particularly difficult in the produce industry as employees are often seasonal or temporary contract employees; thus a strategy of repetitive training is often needed.
Recent research has demonstrated that unsanitary packinghouse facility equipment may play a major role in contaminating fresh fruits and vegetables if packinghouse facility food contact surfaces such as conveyor belts and dump tanks that convey produce are not cleaned and sanitized on a regularly scheduled basis with food contact surface approved cleaning compounds [42,43]. Sanitizers to be effective should be used only after thorough cleaning with mechanical action to remove organic materials such as dirt or plant materials. Food processing plants and equipment associated with them are normally designed with wash-down sanitation in mind. However, sanitary design of facilities and equipment used to handle raw agricultural commodities has received only limited attention. Therefore, there are currently no universally accepted standards for equipment or sanitary design for facilities that handle raw agricultural commodities. Rough postharvest handling at packinghouse facilities should be avoided to reduce mechanical damage and punctures to fruit which may allow for the introduction of plant spoilage pathogens via these wounds, as this has been demonstrated to enhance the potential for growth and survival of some human pathogens .
All water that comes in contact with produce for drenching, washing, hydro-cooling, or vacuum cooling must be of sufficient microbial quality to prevent contamination. Recirculated water should have sufficient quantities of an approved wash water disinfectant to reduce the potential for cross contamination of all produce in the drenching, washing, or hydrocooling system. Wash water disinfectants are not capable of sterilizing the surface of produce. Research has demonstrated that washing produce in cold chlorinated water will reduce microbial populations by two or three log units (100- to 1000-fold), but complete elimination of microbes is never achieved because microorganisms adhere so tenaciously to the surface of produce and may be present in microscopic hydrophobic areas on the produce surface [2,3] or in inaccessible attachment sites (stomata, lenticels, punctures). Rinsing produce with water that contains a wash water disinfectant will significantly reduce the number of microorganisms present on the produce but it will not remove or inactivate all bacteria. Human pathogens cannot be completely removed from produce by washing in cold chlorinated water [20,45]. (See Chapter 17 for more details.)
It is particularly important that water used for hydrocooling produce be free of pathogenic microorganisms, as when warm produce is placed in cold water, intercellular air spaces within fruits and vegetables contract, creating a partial vacuum (pressure differential). This has been demonstrated to facilitate infiltration of water, which may contain human pathogens, into fresh produce items. While this phenomenon is known to be an important source of plant pathogen infections during postharvest handling of fruit and vegetables [46-49], only recently has direct evidence been brought forward to show that human pathogens may enter produce by this same mechanism. In a follow-up investigation of potential sources of imported mango contamination, Penteado et al.  provided evidence that Salmonella spp. may be internalized in fresh mangoes during simulated postharvest hot water insect disinfestation procedures which included a water bath cooling step . However, Richards and Beuchat  demonstrated that adhering to or infiltrating of S. Poona cells into cantaloupe tissue via the stem scar is not dictated entirely by the temperature differential between the melon and the immersion solution containing salmonella cells, but it is also influenced by properties unique to tissue surfaces.
Cold storage facilities and, in particular, refrigeration coils, refrigeration drip pans, forced air cooling fans, drain tiles, walls, and floors are potential harborages for human pathogens and as such should be cleaned and sanitized on a frequent and regular basis. Listeria monocytogenes can proliferate quite slowly at refrigerated temperatures and may contaminate cold stored produce if condensation from refrigeration units or the ceiling drips onto produce. Placing warm produce with field heat into a cold room with insufficient refrigeration capacity will cause a temperature rise in the room and, as the room cools, a fog or mist may occur. As the water condenses out of the air and onto surfaces of walls and ceilings that harbor human pathogens, contaminated condensate may end up dripping onto the stored produce. Therefore, it is imperative that sufficient cooling capacity is available when cooling produce.
Since packaging materials come in direct contact with fresh fruits and vegetables, they may serve as a potential source of contamination. Packages such as boxes and plastic bags require storage in such a manner as to protect them from insects, rodents, dust, dirt, and other potential sources of contamination. All packaging materials cannot be stored inside enclosed facilities due to space constraints. However, if packaging materials are stored outside an enclosed building, sufficient precautions should be taken to reduce the probability of rodent/animal infestation, and measures should be taken to allow for easily identifiable indicators of an infestation. Plastic field bins and totes are preferred to wooden containers, since plastic surfaces are more amenable to cleaning and sanitizing, which should be done after every use to reduce the potential for cross contamination. Wooden containers or field totes are almost impossible to surface sanitize since they have a porous surface. Cardboard field bins if reused should be visually inspected for cleanliness and lined with a polymeric plastic bag before reuse to prevent the potential risk of cross contamination.
188.8.131.52 Modified Atmosphere Packaging of Fresh Produce
The risk of Clostridium botulinum on ready-to-eat modified atmosphere packaged (MAP) fresh-cut fruits and vegetables has been investigated extensively by a number of research groups in recent years [53-57]. C. botulinum is a spore-forming bacterium commonly found in agricultural environs. Under suitable environmental conditions (temperatures above 5° C, low oxygen conditions, and a pH above 4.6) this microorganism may produce a deadly toxin. Recent research efforts have examined C. botulinum risk factors for various fresh-cut MAP produce. In general, overt gross spoilage of fresh-cut produce occurs well before toxin is produced on shredded cabbage, shredded lettuce, broccoli florets, sliced carrots, and rutabaga. The endemic microflora on fresh-cut produce play an important role in signaling the end of shelf life and are also believed to suppress toxin production by C. botulinum
. However, some products such as butternut squash and onions have been demonstrated under temperature abuse conditions to have the potential of appearing acceptable although containing botulinal toxin . The important interaction between MAP and microbial food safety must always be considered, and continued research efforts to understand fully these relationships are currently underway. An in-depth assessment of the risk of botulism contributed by MAP of fresh-cut produce may be found in Gorny et al. . Several studies at research institutes have found that MAP technologies commonly used in the fresh-cut industry have varying effects on the survival and growth of E. coli O157:H7, Salmonella spp., Shigella spp., and L. monocytogenes [60-63]. While some pathogenic strains may be inhibited, others are unaffected, weakly inhibited, or even stimulated. Because L. monocytogenes can grow at refrigeration temperatures, there is concern that low inoculum levels, coupled with extended shelf life obtained by the use of MAP, may allow L. monocytogenes to proliferate to infectious dosages late in shelf life. The FDA recently reviewed the risk associated with consumption of fresh fruits and vegetables as well as 20 other ready-to-eat food categories and published, as a draft, a risk assessment on the relationship between foodborne L. monocytogenes and human health (www.fda.gov). Risk from human pathogens due to the use of MAP must be assessed on a per product basis. This is due to the complex interactions between the produce, the indigenous microflora, the pathogen, and its environment. An excellent example of this interaction is the inhibitory effect of carrot extract on growth of L. monocytogenes . Due to these complex interactions, broad generalities cannot be drawn regarding the risk of specific human pathogens on various fresh-cut fruits or vegetables and interactions with MAP.
184.108.40.206 Refrigerated Transport, Distribution, and Cold Storage
Produce is best shipped in temperature-controlled refrigerated vehicles. Maintaining perishables at their appropriate temperature when being transported to destination markets will extend shelf life. When appropriate, holding fresh fruits and vegetables at or below 5°C will significantly reduce the growth rate of microbes including human pathogens. However, cold temperatures and high relative humidity conditions which are often optimal for shelf life extension of fresh fruits and vegetables may actually help favor the viability of some human pathogens such as viral particles.
Trucks used during transportation are also a potential source of contamination from human pathogens. Therefore, trucks should be routinely cleaned and sanitized on a regular basis, and trucks that have been used to transport live animals, animal products, or toxic materials should not be used to transport produce or used only after effective cleaning and sanitation.
1.5.3 Food Safety Risk Factors Associated with Foodservice, Restaurant, and Retail Food Stores Handling of Produce
In 2003 the FDA collected data via site visits to over 900 establishments representing nine distinct facility types including restaurants, institutional foodservice operations, and retail food stores. Direct observations of produce handling practices were supplemented with information gained from discussions with management and food workers and were used to document the establishments' compliance status based on provisions in the 1997 Model FDA Food Code .
Failure to control product holding temperatures, poor personal hygiene, use of contaminated equipment/failure to protect food handling equipment from contamination, and risk of potential chemical contamination were the risk factors found to be most often out of compliance with the 1997 FDA Model Food Code. The percentages of "out of compliance" observations for each of these risk factors were found to be: improper holding time/ temperature (49.3%), poor personal hygiene (22.3%), contaminated equipment (20.5%), and chemical contamination (13.5%). Specifically, for the improper holding time and temperature risk factor, it was found that maintaining cold holding temperatures at or below 5°C (41°F) for produce items that are classified as potentially hazardous foods (PHFs) did not occur in 70.2% of the observed situations. Holding PHFs at or below 5°C (41°F) is critical to preventing the potential growth of human pathogens, which may rapidly proliferate on inadequately refrigerated PHFs. Date marking of refrigerated ready-to-eat PHFs is also an important component of any food safety system, and it is designed to promote proper food rotation and limit the growth of L. monocytogenes during cold storage. However, appropriate date marking of ready-to eat PHF produce items made on-site did not occur in 34% of the observations.
The personal hygiene risk factors associated with produce that are most in need of attention at retail and foodservice operations include adequate, available, and accessible hand washing facilities. These personal hygiene risk factors were found by the survey to be not in compliance with the 1997 FDA Model Food Code 33.3, 26.2, and 20.6% of the time, respectively. Hands are very common vehicles for the transfer of human pathogens to food products, and food handlers' hands may become contaminated when they engage in activities such as handling raw meat products, using the lavatory, coughing, or handling soiled tableware.
Food safety procedures for cleaning and sanitizing food contact surfaces and utensils for handling produce were found to be not in compliance with the 1997 FDA Model Food Code in 44.4% of the observations in this study. Proper cleaning and sanitization of food contact surfaces is essential to preventing cross contamination. The 2004 FDA report clearly indicates that foodservice and retail operators must ensure that their produce food safety management systems are designed to achieve active managerial control over the risk factors associated with handling produce identified in the report.
1.5.4 Consumer Handling of Produce from Purchase to Plate
Li-Cohen and Bruhn  in 2002 published the most extensive consumer handling study of fresh produce from the time of purchase to the plate. Via a national mail survey of 624 respondents these researchers quantified consumer produce handling practices as they relate to food safety risk. Six percent of consumer respondents replied that they never or seldom wash fresh produce before consumption, and greater than 35% of respondents do not wash melons before consumption. Approximately half of all respondents did not wash their hands before handling fresh produce. Ninety-seven percent of all respondents reported that they always washed food preparation surfaces after contact with raw meat products. However, 5% of respondents only dry wipe, and 24% of respondents wash these potentially contaminated food preparation surfaces only with water (without soap or a disinfectant). This survey also found that many respondents did not separate produce from raw meat, poultry, or fish in their refrigerators. These limited observations clearly indicate the need for educational outreach to consumers that must emphasize safe handling practices of produce from purchase to consumption.
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